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The Journal of Maternal-Fetal & Neonatal Medicine Volume 31, 2018 - Issue 4
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Original Article

Intra-amniotic administration of lipopolysaccharide induces spontaneous preterm labor and birth in the absence of a body temperature change

Nardhy Gomez-LopezPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD, and Detroit, MI, USA; ;Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA; ;Department of Immunology and Microbiology, Wayne State University School of Medicine, Detroit, MI, USA; Correspondence[email protected]
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Roberto RomeroPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD, and Detroit, MI, USA; ;Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, MI, USA; ;Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, USA; ;Center for Molecular Medicine and Genetics, Wayne State University, Detroit, MI, USACorrespondence[email protected]
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Marcia Arenas-HernandezPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD, and Detroit, MI, USA; ;Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA; View further author information
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Bogdan PanaitescuPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD, and Detroit, MI, USA; ;Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA; View further author information
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Valeria Garcia-FloresPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD, and Detroit, MI, USA; ;Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA; View further author information
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Tara N. MialPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD, and Detroit, MI, USA; ;Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA; View further author information
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Aashna SahiDepartment of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA; View further author information
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Sonia S. HassanPerinatology Research Branch, Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, MD, and Detroit, MI, USA; ;Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA; View further author information
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Pages 439-446 | Received 07 Jul 2016, Accepted 24 Jan 2017, Published online: 23 Feb 2017

Citations (42)

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Jaroslav Stranik, Marian Kacerovsky, Peter Vescicik, Tomas Faist, Bo Jacobsson & Ivana Musilova. (2022) A rodent model of intra-amniotic inflammation/infection, induced by the administration of inflammatory agent in a gestational sac, associated with preterm delivery: a systematic review. The Journal of Maternal-Fetal & Neonatal Medicine 35:8, pages 1592-1600.
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George Schwenkel, Roberto Romero, Rebecca Slutsky, Kenichiro Motomura, Chaur-Dong Hsu & Nardhy Gomez-Lopez. (2021) HSP70: an alarmin that does not induce high rates of preterm birth but does cause adverse neonatal outcomes. The Journal of Maternal-Fetal & Neonatal Medicine 34:24, pages 4110-4118.
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Hassendrini N. Peiris, Roberto Romero, Kanchan Vaswani, Sarah Reed, Nardhy Gomez-Lopez, Adi L. Tarca, Dereje W. Gudicha, Offer Erez, Eli Maymon & Murray D. Mitchell. (2021) Preterm labor is characterized by a high abundance of amniotic fluid prostaglandins in patients with intra-amniotic infection or sterile intra-amniotic inflammation. The Journal of Maternal-Fetal & Neonatal Medicine 34:24, pages 4009-4024.
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Articles from other publishers (39)

Jose Galaz, Roberto Romero, Jonathan M. Greenberg, Kevin R. Theis, Marcia Arenas-Hernandez, Yi Xu, Marcelo Farias-Jofre, Derek Miller, Tomi Kanninen, Valeria Garcia-Flores & Nardhy Gomez-Lopez. (2023) Host-microbiome interactions in distinct subsets of preterm labor and birth. iScience 26:12, pages 108341.
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Marcelo Farias-Jofre, Roberto Romero, Jose Galaz, Yi Xu, Derek Miller, Valeria Garcia-Flores, Marcia Arenas-Hernandez, Andrew D. Winters, Bruce A. Berkowitz, Robert H. Podolsky, Yimin Shen, Tomi Kanninen, Bogdan Panaitescu, Catherine R. Glazier, Roger Pique-Regi, Kevin R. Theis & Nardhy Gomez-Lopez. (2023) Blockade of IL-6R prevents preterm birth and adverse neonatal outcomes. eBioMedicine 98, pages 104865.
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Neeraja Purandare, Nardhy Gomez-Lopez, Marcia Arenas-Hernandez, Jose Galaz, Roberto Romero, Yue Xi, Andrew M. Fribley, Lawrence I. Grossman & Siddhesh Aras. (2023) The MNRR1 activator nitazoxanide abrogates lipopolysaccharide-induced preterm birth in mice. Placenta 140, pages 66-71.
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Valeria Garcia-Flores, Roberto Romero, Azam Peyvandipour, Jose Galaz, Errile Pusod, Bogdan Panaitescu, Derek Miller, Yi Xu, Li Tao, Zhenjie Liu, Adi L. Tarca, Roger Pique-Regi & Nardhy Gomez-Lopez. (2023) A single-cell atlas of murine reproductive tissues during preterm labor. Cell Reports 42:1, pages 111846.
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Jose Galaz, Roberto Romero, Marcia Arenas-Hernandez, Marcelo Farias-Jofre, Kenichiro Motomura, Zhenjie Liu, Naoki Kawahara, Catherine Demery-Poulos, Tzu Ning Liu, Justin Padron, Bogdan Panaitescu & Nardhy Gomez-Lopez. (2022) Clarithromycin prevents preterm birth and neonatal mortality by dampening alarmin-induced maternal–fetal inflammation in mice. BMC Pregnancy and Childbirth 22:1.
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Neeraja Purandare, Yusef Kunji, Yue Xi, Roberto Romero, Nardhy Gomez-Lopez, Andrew Fribley, Lawrence I. Grossman & Siddhesh Aras. (2022) Lipopolysaccharide induces placental mitochondrial dysfunction in murine and human systems by reducing MNRR1 levels via a TLR4-independent pathway. iScience 25:11, pages 105342.
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Jonathan M. Greenberg, Roberto Romero, Andrew D. Winters, Jose Galaz, Valeria Garcia-Flores, Marcia Arenas-Hernandez, Jonathan Panzer, Zachary Shaffer, David J. Kracht, Nardhy Gomez-Lopez & Kevin R. Theis. (2022) Microbiota of the Pregnant Mouse: Characterization of the Bacterial Communities in the Oral Cavity, Lung, Intestine, and Vagina through Culture and DNA Sequencing. Microbiology Spectrum 10:4.
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Kenichiro Motomura, Roberto Romero, Jose Galaz, Li Tao, Valeria Garcia-Flores, Yi Xu, Bogdan Done, Marcia Arenas-Hernandez, Derek Miller, Pedro Gutierrez-Contreras, Marcelo Farias-Jofre, Siddhesh Aras, Lawrence I. Grossman, Adi L. Tarca & Nardhy Gomez-Lopez. (2022) Fetal and maternal NLRP3 signaling is required for preterm labor and birth. JCI Insight 7:16.
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Dereje W. Gudicha, Roberto Romero, Nardhy Gomez-Lopez, Jose Galaz, Gaurav Bhatti, Bogdan Done, Eunjung Jung, Dahiana M. Gallo, Mariachiara Bosco, Manaphat Suksai, Ramiro Diaz-Primera, Piya Chaemsaithong, Francesca Gotsch, Stanley M. Berry, Tinnakorn Chaiworapongsa & Adi L. Tarca. (2022) The amniotic fluid proteome predicts imminent preterm delivery in asymptomatic women with a short cervix. Scientific Reports 12:1.
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Jaroslav Stranik, Marian Kacerovsky, Martin Sterba, Ctirad Andrys, Cilia Abad, Frantisek Staud, Stanislav Micuda, Ondrej Soucek, Bo Jacobsson & Ivana Musilova. (2022) Development of a Rat Model of Intra-Amniotic Inflammation via Ultrasound-Guided Administration of a Triggering Agent in the Gestational Sac to Enable Analysis of Individual Amniotic Fluid Samples. Frontiers in Pharmacology 13.
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Tik Muk, Allan Stensballe, Oksana Dmytriyeva, Anders Brunse, Ping-Ping Jiang, Thomas Thymann, Per Torp Sangild & Stanislava Pankratova. (2022) Differential Brain and Cerebrospinal Fluid Proteomic Responses to Acute Prenatal Endotoxin Exposure. Molecular Neurobiology 59:4, pages 2204-2218.
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Tiphaine Raia-Barjat, Margaux Digonnet, Antoine Giraud, Taghreed Ayash, Seline Vancolen, Mohamed Benharouga, Céline Chauleur, Nadia Alfaidy & Guillaume Sébire. (2022) Animal Models of Chorioamnionitis: Considerations for Translational Medicine. Biomedicines 10:4, pages 811.
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Kenichiro Motomura, Roberto Romero, Olesya Plazyo, Valeria Garcia-Flores, Meyer Gershater, Jose Galaz, Derek Miller & Nardhy Gomez-Lopez. (2021) The alarmin S100A12 causes sterile inflammation of the human chorioamniotic membranes as well as preterm birth and neonatal mortality in mice. Biology of Reproduction 105:6, pages 1494-1509.
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F. L. Henrique, A. J. Zanella, H. V. A. Bezerra, H. Z. Polato, A. C. Fernandes, H. B. Hooper, L. F. Pulido-Rodríguez, E. A. L. Titto, A. M. F. Pereira & C. G. Titto. (2021) Stress during first gestation of ewes impairs memory and learning of male offspring. Veterinary Research Communications 45:4, pages 251-260.
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Eunjung Jung, Roberto Romero, Bo Hyun Yoon, Kevin R. Theis, Dereje W. Gudicha, Adi L. Tarca, Ramiro Diaz-Primera, Andrew D. Winters, Nardhy Gomez-Lopez, Lami Yeo & Chaur-Dong Hsu. (2021) Bacteria in the amniotic fluid without inflammation: early colonization vs. contamination. Journal of Perinatal Medicine 49:9, pages 1103-1121.
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Nardhy Gomez-Lopez, Valeria Garcia-Flores, Peck Yin Chin, Holly M. Groome, Melanie T. Bijland, Kerrilyn R. Diener, Roberto Romero & Sarah A. Robertson. (2021) Macrophages exert homeostatic actions in pregnancy to protect against preterm birth and fetal inflammatory injury. JCI Insight 6:19.
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Jose Galaz, Roberto Romero, Marcia Arenas-Hernandez, Bogdan Panaitescu, Robert Para & Nardhy Gomez-Lopez. (2021) Betamethasone as a potential treatment for preterm birth associated with sterile intra-amniotic inflammation: a murine study. Journal of Perinatal Medicine 49:7, pages 897-906.
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Amanda Brosius Lutz, Salwan Al-Nasiry, Boris W. Kramer & Martin Mueller. (2021) Understanding Host-Pathogen Interactions in Acute Chorioamnionitis Through the Use of Animal Models. Frontiers in Cellular and Infection Microbiology 11.
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Jang Mee Kim, Seung‐Yun Lee & Ji Yeon Lee. (2021) Melatonin for the prevention of fetal injury associated with intrauterine inflammation. American Journal of Reproductive Immunology 86:1.
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Kenichiro Motomura, Roberto Romero, Jose Galaz, Adi L. Tarca, Bogdan Done, Yi Xu, Yaozhu Leng, Valeria Garcia-Flores, Marcia Arenas-Hernandez, Kevin R. Theis, Meyer Gershater, Eunjung Jung, Chaur-Dong Hsu & Nardhy Gomez-Lopez. (2021) RNA Sequencing Reveals Distinct Immune Responses in the Chorioamniotic Membranes of Women with Preterm Labor and Microbial or Sterile Intra-amniotic Inflammation. Infection and Immunity 89:5.
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Jose Galaz, Roberto Romero, Marcia Arenas-Hernandez, Bogdan Panaitescu, Valeria Garcia-Flores & Nardhy Gomez-Lopez. (2020) A Protocol for Evaluating Vital Signs and Maternal-Fetal Parameters Using High-Resolution Ultrasound in Pregnant Mice. STAR Protocols 1:3, pages 100134.
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Monica Cappelletti, Jessica R. Doll, Traci E. Stankiewicz, Matthew J. Lawson, Vivien Sauer, Bingqiang Wen, Vladimir V. Kalinichenko, Xiaofei Sun, Tamara Tilburgs & Senad Divanovic. (2020) Maternal regulation of inflammatory cues is required for induction of preterm birth. JCI Insight 5:22.
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Hong-yi Zhang, Fang Wang, Xinrao Meng, Chenzhao Feng, Lei Xiang, Gail E. Besner & Jie-xiong Feng. (2020) Prenatal low-dose endotoxin exposure prolongs intestinal epithelial activation after birth and contributes to necrotizing enterocolitis. Journal of Pediatric Surgery 55:11, pages 2308-2316.
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Jang Mee Kim & Ji Yeon Lee. (2020) A Review on the Effects of Melatonin on Fetal Protection during Pregnancy with Intrauterine Inflammation. Journal of The Korean Society of Maternal and Child Health 24:4, pages 196-203.
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Kenichiro Motomura, Roberto Romero, Adi L. Tarca, Jose Galaz, Gaurav Bhatti, Bogdan Done, Marcia Arenas-Hernandez, Dustyn Levenson, Rebecca Slutsky, Chaur-Dong Hsu & Nardhy Gomez-Lopez. (2020) Pregnancy-specific transcriptional changes upon endotoxin exposure in mice. Journal of Perinatal Medicine 48:7, pages 700-722.
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K Motomura, R Romero, V Garcia-Flores, Y Leng, Y Xu, J Galaz, R Slutsky, D Levenson & N Gomez-Lopez. (2020) The alarmin interleukin-1α causes preterm birth through the NLRP3 inflammasome. Molecular Human Reproduction 26:9, pages 712-726.
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Nardhy Gomez-Lopez, Marcia Arenas-Hernandez, Roberto Romero, Derek Miller, Valeria Garcia-Flores, Yaozhu Leng, Yi Xu, Jose Galaz, Sonia S. Hassan, Chaur-Dong Hsu, Harley Tse, Carmen Sanchez-Torres, Bogdan Done & Adi L. Tarca. (2020) Regulatory T Cells Play a Role in a Subset of Idiopathic Preterm Labor/Birth and Adverse Neonatal Outcomes. Cell Reports 32:1, pages 107874.
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Monica Cappelletti, Pietro Presicce & Suhas G. Kallapur. (2020) Immunobiology of Acute Chorioamnionitis. Frontiers in Immunology 11.
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H.N. Basavaprabhu, K.S. Sonu & R. Prabha. (2020) Mechanistic insights into the action of probiotics against bacterial vaginosis and its mediated preterm birth: An overview. Microbial Pathogenesis 141, pages 104029.
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Nardhy Gomez-Lopez, Roberto Romero, George Schwenkel, Valeria Garcia-Flores, Bogdan Panaitescu, Aneesha Varrey, Fatime Ayoub, Sonia S. Hassan & Mark Phillippe. (2020) Cell-Free Fetal DNA Increases Prior to Labor at Term and in a Subset of Preterm Births. Reproductive Sciences 27:1, pages 218-232.
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Caitlin N Cadaret, Elena M Merrick, Taylor L Barnes, Kristin A Beede, Robert J Posont, Jessica L Petersen & Dustin T Yates. (2019) Sustained maternal inflammation during the early third-trimester yields intrauterine growth restriction, impaired skeletal muscle glucose metabolism, and diminished β-cell function in fetal sheep1,2. Journal of Animal Science 97:12, pages 4822-4833.
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Nardhy Gomez‐Lopez, Roberto Romero, Jose Galaz, Yi Xu, Bogdan Panaitescu, Rebecca Slutsky, Kenichiro Motomura, Navleen Gill, Robert Para, Percy Pacora, Eunjung Jung & Chaur‐Dong Hsu. (2019) Cellular immune responses in amniotic fluid of women with preterm labor and intra‐amniotic infection or intra‐amniotic inflammation. American Journal of Reproductive Immunology 82:5.
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Bruce A. Berkowitz, Roberto Romero, Robert H. Podolsky, Karen M. Lins-Childers, Yimin Shen, Tilman Rosales, Youssef Zaim Wadghiri, D. Minh Hoang, Marcia Arenas-Hernandez, Valeria Garcia-Flores, George Schwenkel, Bogdan Panaitescu & Nardhy Gomez-Lopez. (2019) QUEST MRI assessment of fetal brain oxidative stress in utero. NeuroImage 200, pages 601-606.
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Marcia Arenas-Hernandez, Roberto Romero, Yi Xu, Bogdan Panaitescu, Valeria Garcia-Flores, Derek Miller, Hyunyoung Ahn, Bogdan Done, Sonia S. Hassan, Chaur-Dong Hsu, Adi L. Tarca, Carmen Sanchez-Torres & Nardhy Gomez-Lopez. (2019) Effector and Activated T Cells Induce Preterm Labor and Birth That Is Prevented by Treatment with Progesterone. The Journal of Immunology 202:9, pages 2585-2608.
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Nardhy Gomez-Lopez, Roberto Romero, Valeria Garcia-Flores, Yaozhu Leng, Derek Miller, Sonia S Hassan, Chaur-Dong Hsu & Bogdan Panaitescu. (2019) Inhibition of the NLRP3 inflammasome can prevent sterile intra-amniotic inflammation, preterm labor/birth, and adverse neonatal outcomes†. Biology of Reproduction 100:5, pages 1306-1318.
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Jonathan Faro, Roberto Romero, George Schwenkel, Valeria Garcia-Flores, Marcia Arenas-Hernandez, Yaozhu Leng, Yi Xu, Derek Miller, Sonia S Hassan & Nardhy Gomez-Lopez. (2019) Intra-amniotic inflammation induces preterm birth by activating the NLRP3 inflammasome†. Biology of Reproduction 100:5, pages 1290-1305.
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Valeria Garcia-Flores, Roberto Romero, Derek Miller, Yi Xu, Bogdan Done, Chharitha Veerapaneni, Yaozhu Leng, Marcia Arenas-Hernandez, Nabila Khan, Bogdan Panaitescu, Sonia S. Hassan, Luis Marat Alvarez-Salas & Nardhy Gomez-Lopez. (2018) Inflammation-Induced Adverse Pregnancy and Neonatal Outcomes Can Be Improved by the Immunomodulatory Peptide Exendin-4. Frontiers in Immunology 9.
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Ronald McCarthy, Carmel Martin-Fairey, Dorothy K Sojka, Erik D Herzog, Emily S Jungheim, Molly J Stout, Justin C Fay, Mala Mahendroo, Jeff Reese, Jennifer L Herington, Erin J Plosa, Elaine L Shelton & Sarah K England. (2018) Mouse models of preterm birth: suggested assessment and reporting guidelines†. Biology of Reproduction.
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Nardhy Gomez-Lopez, Roberto Romero, Olesya Plazyo, George Schwenkel, Valeria Garcia-Flores, Ronald Unkel, Yi Xu, Yaozhu Leng, Sonia S. Hassan, Bogdan Panaitescu, Jeeyeon Cha & Sudhansu K. Dey. (2017) Preterm labor in the absence of acute histologic chorioamnionitis is characterized by cellular senescence of the chorioamniotic membranes. American Journal of Obstetrics and Gynecology 217:5, pages 592.e1-592.e17.
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