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Enninga, Elizabeth Ann L

0000-0003-3621-7335

Mayo Clinic

Department of Obstetrics and Gynecology, Mayo Clinic, Rochester, Minnesota, USA.

Citations 38

Prevention of the Vertical Transmission of HIV; A Recap of the Journey so Far
Cárdenas, María C. , Farnan, Sheila, Hamel, Benjamin , Plazas, Maria C. Mejia , Sintim-Aboagye, Elise, Littlefield, Dawn, Punia, Sohan, Enninga, Elizabeth Ann L. , Temesgen, Zelalem , Theiler, Regan N. , Gray, Clive M. , Chakraborty, Rana , Cardenas, Maria Camila, Mejia Plazas, Maria Camila, Littlefield, Dawn R, Behl, Supriya, Enninga, Elizabeth Ann L , Theiler, Regan , Gray, Clive M , Chakraborty, Rana , Behl, Supriya , Johnson, Erica L.

Viruses | March 27, 2023 | Volume: 15 | Issue: 4 | Pages: 849

10.3390/v15040849 Get It

In 1989, one in four (25%) infants born to women living with HIV were infected; by the age of 2 years, there was 25% mortality among them due to HIV. These and other pieces of data prompted the development of interventions to offset vertical transmission, including the landmark Pediatric AIDS Clinical Trial Group Study (PACTG 076) in 1994. This study reported a 67.5% reduction in perinatal HIV transmission with prophylactic antenatal, intrapartum, and postnatal zidovudine. Numerous studies since then have provided compelling evidence to further optimize interventions, such that annual transmission rates of 0% are now reported by many health departments in the US and elimination has been validated in several countries around the world. Despite this success, the elimination of HIV’s vertical transmission on the global scale remains a work in progress, limited by socioeconomic factors such as the prohibitive cost of antiretrovirals. Here, we review some of the key trials underpinning the development of guidelines in the US as well as globally, and discuss the evidence through a historic lens.
Fetal surgery is not associated with increased inflammatory placental pathology
Cárdenas, María C. , Cheek‐Norgan, E. Heidi, Norgan, Andrew P. , Schenone, Mauro , Lemens, Maureen A. , Chakraborty, Rana , Ruano, Rodrigo , Enninga, Elizabeth Ann L. , Branda, Megan E. , Ruano, Rodrigo , Enninga, Elizabeth Ann L , Norgan, Andrew P , Schenone, Mauro H

Prenatal Diagnosis | January 23, 2023 | Volume: 43 | Issue: 3 | Pages: 382-392

10.1002/pd.6319 Get It

AbstractObjectiveFetal surgery has improved neonatal outcomes; however, it is unknown if the intervention contributes to the developmental of inflammatory pathologies in the placenta. Here, an association between fetal surgery and placental pathology was examined.MethodThis case‐control study compared pregnancies with fetal surgery (n = 22), pregnancies with an indication for fetal surgery but without an intervention being done (n = 13), and gestational‐age and fetus‐number matched controls (n = 36). Data on maternal, infant, and placental outcomes were abstracted. Additionally, immunohistochemistry identified expression of lymphoid and myeloid cells in the placenta on a subset of cases. Comparisons were performed using Kruskal‐Wallis or Pearson's chi‐squared tests.ResultsMaternal characteristics were comparable between groups. Most fetal interventions were for diaphragmatic hernia, spina bifida, or twin‐to‐twin transfusion syndrome. Fetuses who were operated on before birth were more likely to be born preterm (p = 0.02). There was no increase in the rate of observed placental pathologies or immune cell infiltration in fetal surgery cases compared to controls.ConclusionThe data suggest that fetal surgery is not associated with increased inflammatory or morphologic pathology in the placenta. This observation supports the growing field of fetal surgery.
A Systematic Review to Evaluate a Possible Association Between Congenital Toxoplasmosis and Preterm Labor
Mejia, Maria C., Cárdenas, María C. , Narasimhan, Ramya, Littlefield, Dawn, Enninga, Elizabeth Ann L. , Chakraborty, Rana , Plazas, Maria C. Mejia , Enninga, Elizabeth Ann L

Pediatric Infectious Disease Journal | November 14, 2022 | Volume: 41 | Issue: 12 | Pages: e520-e524

10.1097/inf.0000000000003723 Get It

Background: Congenital toxoplasmosis (CT) is a widespread infection in several countries, and it is defined as an infection of a fetus, newborn, or infant under 1 year of age. Moreover, it represents a thread to pregnant women globally. The objective of our study is to evaluate a potential association between prematurity and CT and whether intrauterine transmission impacts gestational length during pregnancy. Methods: PubMed, Cochrane Library and Google Scholar databases were searched from 1950 to 2019. Case–control studies, retrospective, and prospective cohort studies were eligible. Seven studies were included from a total of 314. The Newcastle–Ottawa scale was used to establish the quality of the articles included. Results: Based on our review, an association between CT and preterm labor was not established, which may reflect heterogeneity in screening, treatments administered, and differing reported incidences of CT across continents over 69 years. A multicenter prospective cohort study powered to investigate a potential association is indicated. Conclusion: Further studies are needed including multicenter prospective cohort studies powered to investigate key clinical associations such as vertical transmission and preterm birth.
Platelet-Derived Exosomes Induce Cell Proliferation and Wound Healing in Human Endometrial Cells
Miller, Colleen , Enninga, Elizabeth Ann L. , Rizzo, Skylar A. , Phillipps, Jordan , Guerrero‐Cazares, Hugo , DeStephano, Christopher C. , Peterson, Timothy E., Stalboerger, Paul G., Khan, Zaraq , Miller, Colleen M , L Enninga, Elizabeth Ann, Enninga, Elizabeth Ann L , Guerrero-Cazares, Hugo , Behfar, Atta

Regenerative Medicine | October 4, 2022 | Volume: 17 | Issue: 11 | Pages: 805-817

10.2217/rme-2022-0095 Get It

Maternal Monocytes Respond to Cell-Free Fetal DNA and Initiate Key Processes of Human Parturition
Kazemi, Nazanin Yeganeh , Fedyshyn, Bohdana , Sutor, Shari L., Fedyshyn, Yaroslav , Markovic, Svetomir N. , Enninga, Elizabeth Ann L. , Yeganeh Kazemi, Nazanin , Sutor, Shari, Markovic, Svetomir , Enninga, Elizabeth Ann L

The Journal of Immunology | October 18, 2021 | Volume: 207 | Issue: 10 | Pages: 2433-2444

10.4049/jimmunol.2100649 Get It

Abstract Throughout gestation, the maternal immune system is tightly modulated to allow growth of a semiallogeneic fetus. During the third trimester, the maternal immune system shifts to a proinflammatory phenotype in preparation for labor. What induces this shift remains unclear. Cell-free fetal DNA (cffDNA) is shed by the placenta and enters maternal circulation throughout pregnancy. Levels of cffDNA are increased as gestation progresses and peak before labor, coinciding with a shift to proinflammatory maternal immunity. Furthermore, cffDNA is abnormally elevated in plasma from women with complications of pregnancy, including preterm labor. Given the changes in maternal immunity at the end of pregnancy and the role of sterile inflammation in the pathophysiology of spontaneous preterm birth, we hypothesized that cffDNA can act as a damage-associated molecular pattern inducing an inflammatory cytokine response that promotes hallmarks of parturition. To test this hypothesis, we stimulated human maternal leukocytes with cffDNA from primary term cytotrophoblasts or maternal plasma and observed significant IL-1β and CXCL10 secretion, which coincides with phosphorylation of IFN regulatory factor 3 and caspase-1 cleavage. We then show that human maternal monocytes are crucial for the immune response to cffDNA and can activate bystander T cells to secrete proinflammatory IFN-γ and granzyme B. Lastly, we find that the monocyte response to cffDNA leads to vascular endothelium activation, induction of myometrial contractility, and PGE2 release in vitro. Our results suggest that the immune response to cffDNA can promote key features of the parturition cascade, which has physiologic consequences relevant to the timing of labor.
Evaluating Markers of Immune Tolerance and Angiogenesis in Maternal Blood for an Association with Risk of Pregnancy Loss
Wyatt, Michelle A. , Baumgarten, Sarah C., Weaver, Amy L. , Oort, Chelsie C. Van, Fedyshyn, Bohdana , Ruano, Rodrigo , Shenoy, Chandra C. , Enninga, Elizabeth Ann L. , Van Oort, Chelsie C, Ruano, Rodrigo , Enninga, Elizabeth Ann L

Journal of Clinical Medicine | August 15, 2021 | Volume: 10 | Issue: 16 | Pages: 3579

10.3390/jcm10163579 Get It

Pregnancy loss affects approximately 20% of couples. The lack of a clear cause complicates half of all miscarriages. Early evidence indicates the maternal immune system and angiogenesis regulation are both key players in implantation success or failure. Therefore, this prospective study recruited women in the first trimester with known viable intrauterine pregnancy and measured blood levels of immune tolerance proteins galectin-9 (Gal-9) and interleukin (IL)-4, and angiogenesis proteins (vascular endothelial growth factors (VEGF) A, C, and D) between 5 and 9 weeks gestation. Plasma concentrations were compared between groups defined based on (a) pregnancy outcome and (b) maternal history of miscarriage, respectively. In total, 56 women were recruited with 10 experiencing a miscarriage or pregnancy loss in the 2nd or 3rd trimester and 11 having a maternal history or miscarriage. VEGF-C was significantly lower among women with a miscarriage or pregnancy loss. Gal-9 and VEGF-A concentrations were decreased in women with a prior miscarriage. Identification of early changes in maternal immune and angiogenic factors during pregnancy may be a tool to improve patient counseling on pregnancy loss risk and future interventions to reduce miscarriage in a subset of women.
Increased cell‐free fetal DNA release after apoptosis and sterile inflammation in human trophoblast cells
Kazemi, Nazanin Yeganeh , Fedyshyn, Bohdana , Yelsa, Isabel, Fedyshyn, Yaroslav , Ruano, Rodrigo , Chakraborty, Rana , Enninga, Elizabeth Ann L. , Enninga, Elizabeth Ann L , Ruano, Rodrigo , Yeganeh Kazemi, Nazanin , Markovic, Svetomir N.

American Journal of Reproductive Immunology | July 7, 2021 | Volume: 86 | Issue: 5 | Pages: No page available

10.1111/aji.13483 Get It

AbstractProblemCell‐free fetal DNA (cffDNA) shed from the placenta can be detected in maternal blood and increases incrementally during gestation. Concentrations are further elevated with pregnancy complications. Specific activators of cffDNA release in such complications have not been identified. Here, we use trophoblast cells from early and term placenta to examine cffDNA release following apoptosis, infection, and sterile inflammatory stress.Method of StudyHTR8/SVneo cells were used to model first‐trimester trophoblasts, and term cytotrophoblasts (CTBs) were isolated from placentae collected after uncomplicated deliveries. Trophoblasts were treated with varying concentrations of doxorubicin (DOX), lipopolysaccharide (LPS), or high‐mobility group box protein 1 (HMGB1) for 18 h. Cells or supernatants were quantified for caspase‐3/7 cleavage, pro‐inflammatory cytokine secretion, and cffDNA release.ResultsBoth HTR8/SVneo and CTBs underwent caspase‐3/7 cleavage following DOX treatment, with HTR8/SVneo cells more sensitive to apoptosis than term CTBs. Apoptotic cells released more cffDNA in a dose‐dependent manner. Treatment with LPS resulted in an increase in pro‐inflammatory IL‐6 release, particularly in term CTBs compared to early trophoblasts; however, LPS did not affect cffDNA release. Lastly, while neither cell released more TNF‐α following stimulation with HMGB1, both HTR8/SVneo and CTBs released significantly more cffDNA in the presence of HMGB1.ConclusionsThese data show that apoptosis and sterile inflammation induced by DOX and HMGB1, respectively, cause an increase in cffDNA concentrations in both first‐trimester and term trophoblasts. Understanding physiologic release of cffDNA during healthy and complicated pregnancy can identify new targets for the diagnosis and treatment of gestational complications.
T-Cell Homeostatic Imbalance in Placentas From Women With Human Immunodeficiency Virus in the Absence of Vertical Transmission
Ikumi, Nadia M. , Pillay, Komala , Tilburgs, Tamara , Malaba, Thokozile R. , Dzanibe, Sonwabile , Enninga, Elizabeth Ann L. , Chakraborty, Rana , Myer, Landon , Jaspan, Heather B. , Gray, Clive M. , Enninga, Elizabeth Ann L , Gray, Clive M , Lamorde, Mohammed , Khoo, Saye

The Journal of Infectious Diseases | April 5, 2021 | Volume: 224 | Issue: Supplement_6 | Pages: S670-S682

10.1093/infdis/jiab192 Get It

Abstract Background Implementation of universal antiretroviral therapy (ART) has significantly lowered vertical transmission rates but has also increased numbers of human immunodeficiency virus (HIV)–exposed uninfected children, who remain vulnerable to morbid effects. In the current study, we investigated whether T-cell alterations in the placenta contribute to altered immune status in HIV-exposed uninfected. Methods We analyzed T cells from term placenta decidua and villous tissue and paired cord blood from pregnant women living with HIV (PWH) who initiated ART late in pregnancy (n = 21) with pregnant women not living with HIV (PWNH) (n = 9). Results Placentas from PWH showed inverted CD4/CD8 ratios and higher proportions of tissue resident CD8+ T cells in villous tissue relative to control placentas. CD8+ T cells in the fetal capillaries, which were of fetal origin, were positively correlated with maternal plasma viremia before ART initiation, implying that imbalanced T cells persisted throughout pregnancy. In addition, the expanded memory differentiation of CD8+ T cells was confined to the fetal placental compartment and cord blood but was not observed in the maternal decidua. Conclusions T-cell homeostatic imbalance in the blood circulation of PWH is reflected in the placenta. The placenta may be a causal link between HIV-induced maternal immune changes during gestation and altered immunity in newborn infants in the absence of vertical transmission.
Placental Immune Responses to Viruses: Molecular and Histo-Pathologic Perspectives
Narang, Kavita , Cheek, Elizabeth, Enninga, Elizabeth Ann L. , Theiler, Regan N. , Cheek, Elizabeth H, Enninga, Elizabeth Ann L , Theiler, Regan , Cheek, Elizabeth H.

International Journal of Molecular Sciences | March 14, 2021 | Volume: 22 | Issue: 6 | Pages: 2921

10.3390/ijms22062921 Get It

As most recently demonstrated by the SARS-CoV-2 pandemic, congenital and perinatal infections are of significant concern to the pregnant population as compared to the general population. These outcomes can range from no apparent impact all the way to spontaneous abortion or fetal infection with long term developmental consequences. While some pathogens have developed mechanisms to cross the placenta and directly infect the fetus, other pathogens lead to an upregulation in maternal or placental inflammation that can indirectly cause harm. The placenta is a temporary, yet critical organ that serves multiple important functions during gestation including facilitation of fetal nutrition, oxygenation, and prevention of fetal infection in utero. Here, we review trophoblast cell immunology and the molecular mechanisms utilized to protect the fetus from infection. Lastly, we discuss consequences in the placenta when these protections fail and the histopathologic result following infection.
Recurrent Gestational Diabetes Mellitus: A Narrative Review and Single-Center Experience
Egan, Aoife M. , Enninga, Elizabeth Ann L. , Alrahmani, Layan , Weaver, Amy L. , Sarras, Michael P. , Ruano, Rodrigo , Ruano, Rodrigo , Egan, A M , Sarras, Michael P , Enninga, Elizabeth Ann L

Journal of Clinical Medicine | February 3, 2021 | Volume: 10 | Issue: 4 | Pages: 569

10.3390/jcm10040569 Get It

Gestational diabetes mellitus (GDM) is a frequently observed complication of pregnancy and is associated with an elevated risk of adverse maternal and neonatal outcomes. Many women with GDM will go on to have future pregnancies, and these pregnancies may or may not be affected by GDM. We conducted a literature search, and based on data from key studies retrieved during the search, we describe the epidemiology of GDM recurrence. This includes a summary of the observed clinical risk factors of increasing maternal age, weight, ethnicity, and requirement for insulin in the index pregnancy. We then present our data from Mayo Clinic (January 2013–December 2017) which identifies a GDM recurrence rate of 47.6%, and illustrates the relevance of population-based studies to clinical practice. Lastly, we examine the available evidence on strategies to prevent GDM recurrence, and note that more research is needed to evaluate the effect of interventions before, during and after pregnancy.