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      Prostacyclin, thromboxane and glomerular filtration rate are abnormal in sickle cell pregnancy

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          Abstract

          Background

          Pregnancy increases the risk of morbidity and mortality in sickle cell disease. We previously showed pregnant women with sickle cell disease to have a relatively low plasma renin concentration in late pregnancy, associated with a lack of the expected plasma volume expansion. We hypothesized this to be due to increased systemic vascular resistance through an imbalance between the vasodilator prostacyclin and vasoconstrictor thromboxane, associated with decreased glomerular filtration rate (GFR).

          Objective

          To compare estimated prostacyclin, thromboxane and GFR in non-pregnant and pregnant women with hemoglobin SS (HbSS) and AA (HbAA).

          Study design

          Four groups of 20 normotensive, nulliparous women were studied in Lagos, Nigeria: pregnant HbSS or HbAA women at 36–40 weeks gestation; non-pregnant HbSS and HbAA controls. We measured stable metabolites of prostacyclin and thromboxane A 2 by enzyme-linked immunosorbent assay; GFR using the Cockcroft-Gault equation. Data analysis was by independent (Student’s) t-test or Mann-Whitney U test for comparisons between any two groups of continuous variables, univariate ANOVA for multiple groups and Pearson’s correlation coefficient for degree of association between variables.

          Results

          HbSS women had lower serum 6-keto-PGF1α concentrations than HbAA, whether pregnant or non-pregnant (P<0.001; P<0.004 respectively). Conversely, pregnant HbSS women had higher serum TxB2 (P<0.001); non-pregnant HbSS women had non-significantly higher TxB2 concentrations. The 6-keto-PGF1α:TxB2 ratio was markedly increased (pro-vasodilatory) in HbAA pregnancy (P<0.001) but reduced in HbSS pregnancy (P = 0.037). GFRs (mL/min) were higher in non-pregnant HbSS than HbAA (P<0.008) but only marginally raised in HbSS women in late pregnancy (P = 0.019) while markedly raised in HbAA pregnancy (P<0.001).

          Conclusion

          The lower ratio of prostacyclin-thromboxane metabolites in HbSS pregnancy may indicate endothelial damage and an increased tendency to vasoconstriction and clotting. If confirmed by subsequent longitudinal studies, interventions to increase prostacyclin and reduce thromboxane, such as low dose aspirin, may be potentially useful in their management.

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          Most cited references32

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          Antiplatelet agents for preventing pre-eclampsia and its complications.

          S Meher, Andrew King, Steven Smart … (2006)
          Pre-eclampsia is associated with deficient intravascular production of prostacyclin, a vasodilator, and excessive production of thromboxane, a vasoconstrictor and stimulant of platelet aggregation. These observations led to the hypotheses that antiplatelet agents, low-dose aspirin in particular, might prevent or delay development of pre-eclampsia. To assess the effectiveness and safety of antiplatelet agents for women at risk of developing pre-eclampsia. We searched the Cochrane Pregnancy and Childbirth Group's Trials Register (July 2006), the Cochrane Central Register of Controlled Trials (The Cochrane Library 2005, Issue 1), EMBASE (1994 to November 2005) and handsearched congress proceedings of the International and European Societies for the Study of Hypertension in Pregnancy. All randomised trials comparing antiplatelet agents with either placebo or no antiplatelet agent were included. Quasi-random studies were excluded. Participants were pregnant women at risk of developing pre-eclampsia. Interventions were any comparisons of an antiplatelet agent (such as low-dose aspirin or dipyridamole) with either placebo or no antiplatelet. Two authors assessed trials for inclusion and extracted data independently. Fifty-nine trials (37,560 women) are included. There is a 17% reduction in the risk of pre-eclampsia associated with the use of antiplatelet agents ((46 trials, 32,891 women, relative risk (RR) 0.83, 95% confidence interval (CI) 0.77 to 0.89), number needed to treat (NNT) 72 (52, 119)). Although there is no statistical difference in RR based on maternal risk, there is a significant increase in the absolute risk reduction of pre-eclampsia for high risk (risk difference (RD) -5.2% (-7.5, -2.9), NNT 19 (13, 34)) compared with moderate risk women (RD -0.84 (-1.37, -0.3), NNT 119 (73, 333)). Antiplatelets were associated with an 8% reduction in the relative risk of preterm birth (29 trials, 31,151 women, RR 0.92, 95% CI 0.88 to 0.97); NNT 72 (52, 119)), a 14% reduction in fetal or neonatal deaths (40 trials, 33,098 women, RR 0.86, 95% CI 0.76 to 0.98); NNT 243 (131, 1,666) and a 10% reduction in small-for-gestational age babies (36 trials, 23,638 women, RR 0.90, 95% CI0.83 to 0.98). There were no statistically significant differences between treatment and control groups for any other outcomes. Antiplatelet agents, largely low-dose aspirin, have moderate benefits when used for prevention of pre-eclampsia and its consequences. Further information is required to assess which women are most likely to benefit, when treatment is best started, and at what dose.
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            The natural history of sickle cell disease.

            Graham Serjeant (2013)
            The term sickle cell disease embraces a group of genetic conditions in which pathology results from the inheritance of the sickle cell gene either homozygously or as a double heterozygote with another interacting gene. The spectrum of resulting conditions is therefore influenced by the geography of individual hemoglobin genes, but in most populations, the commonest genotype at birth is homozygous sickle cell (SS) disease. Because this genotype generally manifests a greater mortality, the relative proportion of sickle cell genotypes is influenced by age as well as the geographical distribution of individual genes.
            Article 0 comments Cited 67 times – based on 0 reviews     Review now
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              Time course of maternal plasma volume and hormonal changes in women with preeclampsia or fetal growth restriction.

              Guillermo Marshall, P Rosso, S Salas … (2006)
              We tested the hypothesis that women with idiopathic fetal growth restriction (FGR) or preeclampsia (PE) have lower concentrations of some water-retaining hormones, such as aldosterone and estradiol, either preceding or concomitant with the onset of the reduced plasma volume described in these women. Plasma volume and serum concentrations of estradiol, progesterone, and aldosterone were measured serially at monthly intervals in 135 pregnant women from week 10 until term. Twenty-three developed idiopathic FGR, 17 had PE, and 95 remained normotensive and delivered normal-size infants (controls). Changes over time for each variable were studied using mixed models. Maternal age, parity, and weight/height at term were similar in all of the groups. Birth weight, body length, and ponderal index were lower in FGR and PE than in controls. Plasma volume increased throughout pregnancy in controls but was lower in FGR and PE from week 14 to 17 until term. Aldosterone values were lower in PE from week 26 to 29 onwards and in FGR after week 34. Progesterone concentrations were higher in PE than either control or FGR from week 18 to 21 until term. In contrast, FGR pregnancies had reduced progesterone and estradiol concentrations after week 34. Progesterone:estradiol ratio was significantly higher only in the PE group. In mothers with idiopathic FGR or PE, less expansion in plasma volume occurred before alterations in hormonal concentrations. We speculate that the early rise in progesterone may have a pathogenic role in the development of preeclampsia.
              Article 0 comments Cited 65 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Opeyemi Abayomi Obilade: Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: Writing – original draftRole: Writing – review & editing
                Alani Suleimon Akanmu: Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Fiona Broughton Pipkin: Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Bosede Bukola Afolabi:
                ORCID: http://orcid.org/0000-0002-7511-7567
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Markus M. Bachschmid: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 7 September 2017
                Publication date Collection: 2017
                Volume: 12
                Issue: 9
                Electronic Location Identifier: e0184345
                Affiliations
                [1 ] Department of Obstetrics and Gynaecology, Lagos University Teaching Hospital, Idi-Araba, Lagos, Nigeria
                [2 ] Department of Obstetrics and Gynaecology, State House Medical Centre, Aso Rock, Asokoro, Abuja, Nigeria
                [3 ] Department of Haematology and Blood Transfusion, College of Medicine, University of Lagos, Idi-Araba, Lagos, Nigeria
                [4 ] Department of Haematology and Blood Transfusion, Lagos University Teaching Hospital, Idi-Araba, Lagos, Nigeria
                [5 ] Department of Obstetrics and Gynaecology, Faculty of Medicine and Health Sciences, University of Nottingham, Nottingham, United Kingdom
                [6 ] Department of Obstetrics and Gynaecology, College of Medicine University of Lagos, Idi-Araba, Lagos, Nigeria
                Boston University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-7511-7567
                Article
                Publisher ID: PONE-D-17-15044
                DOI: 10.1371/journal.pone.0184345
                PMC ID: 5589233
                PubMed ID: 28880908
                SO-VID: 9cf2f948-774a-4242-b55e-0adab65216b3
                Copyright © © 2017 Obilade et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 18 April 2017
                Date accepted : 22 August 2017
                Page count
                Figures: 2, Tables: 2, Pages: 12
                Funding
                The study was internally funded by OAO as it formed part of the requirements towards the part II Fellowship exam of the Faculty of Obstetrics and Gynaecology of the National Postgraduate Medical College of Nigeria. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Women's Health
                Subject: Maternal Health
                Subject: Pregnancy
                Subject: Medicine and Health Sciences
                Subject: Women's Health
                Subject: Obstetrics and Gynecology
                Subject: Pregnancy
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Renal Physiology
                Subject: Glomerular Filtration Rate
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Renal Physiology
                Subject: Glomerular Filtration Rate
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Hormones
                Subject: Lipid Hormones
                Subject: Thromboxane
                Subject: Medicine and Health Sciences
                Subject: Clinical Genetics
                Subject: Genetic Diseases
                Subject: Autosomal Recessive Diseases
                Subject: Sickle Cell Disease
                Subject: Medicine and Health Sciences
                Subject: Hematology
                Subject: Hemoglobinopathies
                Subject: Sickle Cell Disease
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Hormones
                Subject: Lipid Hormones
                Subject: Prostacyclin
                Subject: Medicine and Health Sciences
                Subject: Women's Health
                Subject: Maternal Health
                Subject: Pregnancy
                Subject: Pregnancy Complications
                Subject: Preeclampsia
                Subject: Medicine and Health Sciences
                Subject: Women's Health
                Subject: Obstetrics and Gynecology
                Subject: Pregnancy
                Subject: Pregnancy Complications
                Subject: Preeclampsia
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Biomarkers
                Subject: Creatinine
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Neurochemistry
                Subject: Neurochemicals
                Subject: Eicosanoids
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Neurochemistry
                Subject: Neurochemicals
                Subject: Eicosanoids
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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