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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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“In addition to enhanced maternal-to-fetal transfer, lipids cause inflammatory changes in the placenta most likely through recruitment and activation of macrophages.(79,80) The consequences of this lowgrade chronic placental inflammation are currently unknown, but shaping and priming of the fetal immune response may we…”
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Developmental Programming and Glucolipotoxicity: Insights on Beta Cell Inflammation and Diabetes
Cerf, M. E. (2020) · Metabolites · doi:10.3390/metabo10110444 · Cited by 19
Prenatal inflammation exposure-programmed cardiovascular diseases and potential prevention
Deng, Y., Song, L., Nie, X., Shou, W., & Li, X. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.05.009 · Cited by 18
Preeclampsia and the Kidney: Pathophysiology and Clinical Implications
Dines, V. A., Suvakov, S. R., Kattah, A. G., Vermunt, J. V., Narang, K., Jayachandran, M., Hassan, C. A., Norby, A. M., & Garovic, V. D. (2023) · Comprehensive physiology · doi:10.1002/cphy.c210051 · Cited by 39
“Abnormal blood flow will generate ischemia-reperfusion injury and placental oxidative stress by-products, with the release of inflammatory biomarkers (such as TNF-α , IL-1a, IL-6), and an imbalance of angiogenic factors, PlGF and sFlt-1, leading to the dramatic systemic changes and clinical…”
Rees, A., Richards, O., Chambers, M., Jenkins, B., Cronin, J., & Thornton, C. A. (2022) · Clinical & Experimental Immunology · doi:10.1093/cei/uxac003 · Cited by 22
“Further elevated circulating maternal IL-6 and CRP levels have been reported in pregnant women with obesity [96].”
BackgroundInfluentialCirulli, F., Simone, R. D., Musillo, C., Ajmone‐Cat, M. A., & Berry, A. (2022) · Nutrients · doi:10.3390/nu14153150 · Cited by 18
“However, in the setting of maternal obesity, histopathological evidence of placental inflammation is described suggesting that such immune tolerance may be disrupted [20,27,28].”
BackgroundMade in the Womb: Maternal Programming of Offspring Cardiovascular Function by an Obesogenic Womb
Diniz, M. S., Grilo, L. F., Tocantins, C., Falcão‐Pires, I., & Pereira, S. P. (2023) · Metabolites · doi:10.3390/metabo13070845 · Cited by 17
Pala, Ş., Atılgan, R., & İlhan, N. (2024) · TURKISH JOURNAL OF MEDICAL SCIENCES · doi:10.55730/1300-0144.5789 · Cited by 17
“Pregnancy, therefore, is characterized as an inflammatory process, with an increase in maternal leukocyte activity and proinflammatory cytokines in the body [14,15].”
BackgroundThe morphometry of materno–fetal oxygen exchange barrier in a baboon model of obesity
Samson, J. E., Mari, G., Dick, E. J., Hubbard, G. B., Ferry, R. J., & Schlabritz‐Loutsevitch, N. (2011) · Placenta · doi:10.1016/j.placenta.2011.07.083 · Cited by 17
“Placental inflammation [6], infiltration by macrophages and neutrophils [15–17], altered placental vascular structure [15,17,18], increased placental weight and other ultra-structural changes [18–20] have been reported.”
BackgroundPlacental structure and function in different breeds in horses
Robles, M., Peugnet, P., Valentino, S., Dubois, C., Dahirel, M., Aubrière, M.-C., Reigner, F., Serteyn, D. A., Wimel, L., Couturier‐Tarrade, A., et al. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.11.007 · Cited by 17
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Collateral Damage: Maternal Obesity During Pregnancy Continues to Rise
Davis, A. M. (2020) · Obstetrical & Gynecological Survey · doi:10.1097/ogx.0000000000000734 · Cited by 17
Diabetes Mellitus Complicating Pregnancy
Landon, M. B., Catalano, P. M., & Gabbe, S. G. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-1935-2.00039-9 · Cited by 17
Self-citationParsons, E. C., Patel, K. B., Tran, B. T., & Littman, A. J. (2012) · Maternal and Child Health Journal · doi:10.1007/s10995-012-1092-x · Cited by 17
Vistnes, M., Tapia, G., Mårild, K., Midttun, Ø., Ueland, P. M., Viken, M. K., Magnus, P. M., Berg, J. P., Gillespie, K. M., Skrivarhaug, T., et al. (2017) · American Journal of Reproductive Immunology · doi:10.1111/aji.12802 · Cited by 17
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Dietary fat: a potent microglial influencer
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Sugino, K. Y., Mandala, A., Janssen, R. C., Gurung, S., Trammell, M., Day, M. W., Brush, R. S., Papin, J. F., Dyer, D. W., Agbaga, M., et al. (2022) · Frontiers in Clinical Diabetes and Healthcare · doi:10.3389/fcdhc.2022.945768 · Cited by 17
“An investigation of the chronic pro-inflammatory milieu in placentas from obese 75 pregnancies showed a two- to three-fold increase in resident macrophages (CD68+ and CD14+) and 76 expression of pro-inflammatory cytokines compared with placentas from lean pregnancies (23).”
BackgroundPhengpol, N., Thongnak, L., & Lungkaphin, A. (2022) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-022-00927-z · Cited by 16
“These provoke macrophage infiltration into the placenta, inducing inflammation of the placenta via the promotion of the expression of IL-1, TNF-α, and IL-6 affecting fetal growth and development [8, 41].”
BackgroundThe pathologic changes of human placental macrophages in women with hyperglycemia in pregnancy
Ning, J., Zhang, M., Cui, D., & Yang, H. (2022) · Placenta · doi:10.1016/j.placenta.2022.11.004 · Cited by 17
Rees, A., Richards, O., Allen-Kormylo, A., Jones, N., & Thornton, C. A. (2022) · Clinical & Experimental Immunology · doi:10.1093/cei/uxac023 · Cited by 16
Wang, Z., Chen, Y., Wang, W., Huang, C., Hu, Y., Johnston, L. J., & Wang, F. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.835950 · Cited by 16
Ribeiro, T. A., Breznik, J. A., Kennedy, K. M., Yeo, E., Kennelly, B. K. E., Jazwiec, P. A., Patterson, V. S., Bellissimo, C. J., Anhê, F. F., Schertzer, J. D., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0284972 · Cited by 18
Evaluating Macrophages in Immunotoxicity Testing
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Impact of maternal obesity on the metabolic profiles of pregnant women and their offspring at birth
Désert, R., Canlet, C., Costet, N., Cordier, S., & Bonvallot, N. (2015) · Metabolomics · doi:10.1007/s11306-015-0836-1 · Cited by 18
“inflammation and changes in glucose or amino acid transport rates (Challier et al., 2008; Farley et al., 2010; Jones et al., 2009).”
BackgroundVisiedo, F., Bugatto, F., Carrasco-Fernández, C., Sáez-Benito, A., Mateos, R. M., Cózar‐Castellano, I., Bartha, J. L., & Perdomo, G. (2015) · Placenta · doi:10.1016/j.placenta.2015.01.199 · Cited by 16
“Obesity in pregnancy induces placental inflammation, which is associated with production of pro-inflammatory mediators [5].”
BackgroundGirchenko, P. V., Lahti‐Pulkkinen, M., Lipsanen, J. O., Heinonen, K., Lahti, J. M. T., Rantalainen, V. J., Hämäläinen, E. K., Laivuori, H. M., Villa, P., Kajantie, E., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01723-3 · Cited by 15
Musumeci, A., McElwain, C. J., Manna, S., McCarthy, F. P., & McCarthy, C. (2024) · Clinical & Experimental Immunology · doi:10.1093/cei/uxae010 · Cited by 20
“This increase has also been reported in placental inflammation in pregnant women with obesity [57], additionally, we have shown that elevated production of mitochondrial superoxide by placental macrophage populations contributes to increased inflammation in GDM [58].”
Alvarado, F., Calabuig-Navarro, V., Haghiac, M., Puchowicz, M., Tsai, P.-J. S., & O’Tierney-Ginn, P. (2018) · Placenta · doi:10.1016/j.placenta.2018.07.016 · Cited by 15
Jaramillo-Ospina, A. M., Castaño‐Moreno, E., Muñoz‐Muñoz, E., Krause, B. J., Uauy, R. D., Casanello, P. C., & Castro-Rodríguez, J. A. (2021) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000003172 · Cited by 15
Kelly, A. C., Rosario, F. J., Chan, J., Cox, L. A., Powell, T. L., & Jansson, T. (2022) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00263.2021 · Cited by 14
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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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