{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,7]],"date-time":"2026-04-07T10:00:31Z","timestamp":1775556031379,"version":"3.50.1"},"reference-count":38,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,4,7]],"date-time":"2026-04-07T00:00:00Z","timestamp":1775520000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,4,7]],"date-time":"2026-04-07T00:00:00Z","timestamp":1775520000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Lab Anim Res"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Preeclampsia is a multisystem pregnancy disorder that is a major contributor to maternal and neonatal morbidity and mortality worldwide. An animal model facilitates further understanding of the disorder and allows for the investigation of targeted therapies prior to first in-human studies. Although there are several animal models for studying preeclampsia, the utero-placental ischemia (UPI) model is thought to best replicate the placental ischemia that develops as preeclampsia evolves in humans. An established non-human primate (NHP) model of UPI resembles human preeclampsia and has been important in understanding and finding cures for this disorder. To date the ischemia in most animal models has been undertaken by surgical ligation of a uterine artery. There are however alternate means to reduce arterial blood flow via endovascular means. This study aimed to investigate the difference between the surgical reduction in flow (surgical UPI) to the use of percutaneously delivered intra-arterial coils (coils UPI).<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      There was no significant difference between the two methods of inducing UPI for the measured parameters: circulating soluble fms-like tyrosine kinase-1(sFLT-1), blood pressure (BP) and proteinuria (\n                      <jats:italic>p<\/jats:italic>\n                      \u2009&lt;\u20090.05). The results showed a percentage change from baseline in sFLT-1 of 3176\u2009\u00b1\u20091558% for the embolization and 2040\u2009\u00b1\u20091645% for the ligation group\n                      <jats:italic>p<\/jats:italic>\n                      \u2009=\u20090.11, three days post-UPI induction. Moreover, there was no difference between the two models in terms of preeclampsia-defining features.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>No statistically significant difference was found between the two methods, coils for endovascular embolization and surgical UPI. However, since endovascular embolization is a less invasive technique compared to ligation it may be preferred for induction of UPI in the NHP model.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s42826-026-00276-8","type":"journal-article","created":{"date-parts":[[2026,4,7]],"date-time":"2026-04-07T09:17:55Z","timestamp":1775553475000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Endovascular coil embolization compared to surgical ligation of the uterine artery in a non-human primate model in a model of preeclampsia"],"prefix":"10.1186","volume":"42","author":[{"given":"A.","family":"Makris","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-8224-7457","authenticated-orcid":false,"given":"N.","family":"Roshan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"Iliopoulos","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"R.","family":"Waugh","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"A.","family":"Al-Hindawi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"B.","family":"Corbett","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C.C.","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"B.","family":"Lian","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S.","family":"Heffernan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"Hyett","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"Ardui","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S.","family":"Pears","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S.A.","family":"Karumanchi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"A.","family":"Hennessy","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2026,4,7]]},"reference":[{"key":"276_CR1","doi-asserted-by":"crossref","unstructured":"Chappell LC, Cluver CA, Kingdom J, Tong S. Pre-eclampsia. 2021;398(10297):341\u201354.","DOI":"10.1016\/S0140-6736(20)32335-7"},{"key":"276_CR2","doi-asserted-by":"publisher","first-page":"102525","DOI":"10.1016\/j.bpobgyn.2024.102525","volume":"96","author":"R Soundararajan","year":"2024","unstructured":"Soundararajan R, Khan T, Dadelszen P. Pre-eclampsia challenges and care in low and middle-income countries: understanding diagnosis, management, and health impacts in remote and developing regions. Best Pract Res Clin Obstet Gynaecol. 2024;96:102525.","journal-title":"Best Pract Res Clin Obstet Gynaecol"},{"key":"276_CR3","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.preghy.2021.09.008","volume":"27","author":"LA Magee","year":"2022","unstructured":"Magee LA, Brown MA, Hall DR, Gupte S, Hennessy A, Karumanchi A, et al. The 2021 International society for the study of hypertension in pregnancy classification, diagnosis & management recommendations for international practice. Pregnancy Hypertens. 2022;27:148\u201369.","journal-title":"Pregnancy Hypertens"},{"issue":"14","key":"276_CR4","doi-asserted-by":"publisher","first-page":"1690","DOI":"10.1016\/j.jacc.2020.08.014","volume":"76","author":"CW Ives","year":"2020","unstructured":"Ives CW, Sinkey R, Rajapreyar I, Tita ATN, Oparil S. Preeclampsia-pathophysiology and clinical presentations. J Am Coll Cardiol. 2020;76(14):1690\u2013702.","journal-title":"J Am Coll Cardiol"},{"issue":"2","key":"276_CR5","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1161\/hy02t2.102904","volume":"39","author":"RL Davisson","year":"2002","unstructured":"Davisson RL, Hoffmann DS, Butz GM, Aldape G, Schlager G, Merrill DC, et al. Discovery of a spontaneous genetic mouse model of preeclampsia. Hypertension. 2002;39(2):337\u201342.","journal-title":"Hypertension"},{"key":"276_CR6","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1095\/biolreprod.106.053603","volume":"75","author":"A Dokras","year":"2006","unstructured":"Dokras A, Hoffmann DS, Eastvold JS, Kienzle MF, Gruman LM, Kirby PA, et al. Severe feto-placental abnormalities precede the onset of hypertension and proteinuria in a mouse model of preeclampsia. Bio Reprod. 2006;75:899\u2013907.","journal-title":"Bio Reprod"},{"key":"276_CR7","doi-asserted-by":"publisher","first-page":"2574","DOI":"10.1096\/fj.201701008R","volume":"32","author":"JL Sones","year":"2018","unstructured":"Sones JL, Merriam AA, Seffens A, Brown-Grant DA, Butler SD, Zhao AM, et al. Angiogenic factor imbalance precedes complement deposition in placentae of the BPH\/5 model of preeclampsia. Faseb J. 2018;32:2574\u201386.","journal-title":"Faseb J"},{"key":"276_CR8","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1161\/HYPERTENSIONAHA.118.10858","volume":"72","author":"AS Care","year":"2018","unstructured":"Care AS, Bourque SL, Morton JS, Hjartarson EP, Robertson SA, Davidge ST. Reduction in regulatory T cells in early pregnancy causes uterine artery dysfunction in mice. Hypertens. 2018;72:177\u201387.","journal-title":"Hypertens"},{"key":"276_CR9","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1016\/S0895-7061(01)02255-5","volume":"15","author":"BT Alexander","year":"2002","unstructured":"Alexander BT, Cockrell KL, Massey MB, Bennett WA, Granger JP. Tumor necrosis factor-alpha-induced hypertension in pregnant rats results in decreased renal neuronal nitric oxide synthase expression. Am J Hypertens. 2002;15:170\u201375.","journal-title":"Am J Hypertens"},{"key":"276_CR10","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1016\/0002-9378(94)90463-4","volume":"171","author":"MM Faas","year":"1994","unstructured":"Faas MM, Schuiling GA, Baller JF, Visscher CA, Bakker WW. A new animal model for human preeclampsia: ultra-low-dose endotoxin infusion in pregnant rats. Am. J. Obstet Gynecol. 1994;171:158\u201364.","journal-title":"Am. J. Obstet Gynecol"},{"key":"276_CR11","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1084\/jem.20130295","volume":"211","author":"T Cotechini","year":"2014","unstructured":"Cotechini T, Komisarenko M, Sperou A, Macdonald-Goodfellow S, Adams MA, Graham CH. Inflammation in rat pregnancy inhibits spiral artery remodeling leading to fetal growth restriction and features of preeclampsia. The J Exp Med. 2014;211:165\u201379.","journal-title":"The J Exp Med"},{"key":"276_CR12","doi-asserted-by":"publisher","first-page":"1686","DOI":"10.3324\/haematol.2019.226209","volume":"105","author":"C Han","year":"2020","unstructured":"Han C, Wang C, Chen Y, Wang J, Xu X, Hilton T, et al. Placenta derived extracellular vesicles induce preeclampsia in mouse models. Haematologica. 2020;105:1686\u201394.","journal-title":"Haematologica"},{"key":"276_CR13","doi-asserted-by":"crossref","unstructured":"Intapad S, Warrington JP, Spradley FT, Palei AC, Drummond HA, Ryan MJ, et al. Reduced uterine perfusion pressure induces hypertension in the pregnant mouse. Am J Physiol Regul Integr Comp Physiol. 2014;307:R1353\u20137.","DOI":"10.1152\/ajpregu.00268.2014"},{"key":"276_CR14","doi-asserted-by":"publisher","first-page":"1191","DOI":"10.1161\/01.HYP.37.4.1191","volume":"37","author":"BT Alexander","year":"2001","unstructured":"Alexander BT, Kassab SE, Miller MT, Abram SR, Reckelhoff JF, Bennett WA, et al. Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertens. 2001;37:1191\u201395.","journal-title":"Hypertens"},{"key":"276_CR15","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1038\/sj.ki.5002175","volume":"71","author":"A Makris","year":"2007","unstructured":"Makris A, Thornton C, Thompson J, Thomson S, Martin R, Ogle R, et al. Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int. 2007;71:977\u201384.","journal-title":"Kidney Int"},{"issue":"6","key":"276_CR16","doi-asserted-by":"publisher","first-page":"1263","DOI":"10.1161\/HYPERTENSIONAHA.116.07286","volume":"67","author":"A Makris","year":"2016","unstructured":"Makris A, Yeung KR, Lim SM, Sunderland N, Heffernan S, Thompson JF, et al. Placental growth factor reduces blood pressure in a uteroplacental ischemia model of preeclampsia in nonhuman primates. Hypertension. 2016;67(6):1263\u201372.","journal-title":"Hypertension"},{"issue":"1","key":"276_CR17","doi-asserted-by":"publisher","first-page":"012003","DOI":"10.1088\/2516-1091\/ab6c7d","volume":"2","author":"CY Wang","year":"2020","unstructured":"Wang CY, Hu J, Sheth RA, Oklu R. Emerging embolic Agents in endovascular embolization: an overview. Prog Biomed Eng (Bristol). 2020;2(1):012003.","journal-title":"Prog Biomed Eng (Bristol)"},{"key":"276_CR18","first-page":"900","volume":"102","author":"SX Loh","year":"2023","unstructured":"Loh SX, Brilakis E, Gasparini G, Agostoni P, Garbo R, Mashayekhi K, et al. Coils embolization use for coronary procedures: basics, indications, and techniques. Catheter Cardiovasc Interv. 2023;102:900\u201311.","journal-title":"Catheter Cardiovasc Interv"},{"key":"276_CR19","doi-asserted-by":"crossref","unstructured":"Belavadi R, Gudigopuram SVR, Raguthu CC, Gajjela H, Kela I, Kakarala CL, et al. Surgical clipping versus endovascular coiling in the management of intracranial aneurysms. Cureus. 2021;13(12):e20478.","DOI":"10.7759\/cureus.20478"},{"key":"276_CR20","first-page":"100708","volume":"21","author":"M Ghorbani","year":"2020","unstructured":"Ghorbani M, Griessenauer CJ, Wipplinger C, Nouri M, Asaadi S, Hejazian E, et al. Surgical clipping compared to endovascular coiling of ruptured coil able middle cerebral aneurysms: a single-center experience. Inter Discip Neuro Surg. 2020;21:100708.","journal-title":"Inter Discip Neuro Surg"},{"issue":"6","key":"276_CR21","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1177\/1591019918792231","volume":"24","author":"C Schwartz","year":"2018","unstructured":"Schwartz C, Aster HC, Al-Schameri R, M\u00fcller-Thies-Broussalis E, Griessenauer CJ, Killer-Oberpfalzer M. Microsurgical clipping and endovascular treatment of middle cerebral artery aneurysms in an interdisciplinary treatment concept: comparison of long-term results. Interv Neuro Radiol. 2018;24(6):608\u201314.","journal-title":"Interv Neuro Radiol"},{"key":"276_CR22","unstructured":"National Health and Medical Research Council. The 3Rs - replacement, reduction and refinement. NHMRC. https:\/\/www.nhmrc.gov.au\/research-policy\/ethics\/animal-ethics\/3rs. 18 Sep 2025."},{"key":"276_CR23","unstructured":"Data Sciences International. Understanding the Ponemah activity Derived Parameter. DSI Support Center. https:\/\/support.datasci.com\/hc\/en-us\/articles\/115005030328-Understanding-the-Ponemah-Activity-Derived-Parameter. 23 Sep 2025."},{"key":"276_CR24","unstructured":"Association of primate veterinarians blood collection guidelines. J Am Assoc Lab Anim Sci. 2022;61(5):403\u201305."},{"key":"276_CR25","doi-asserted-by":"publisher","first-page":"10705","DOI":"10.1073\/pnas.90.22.10705","volume":"90","author":"RL Kendall","year":"1993","unstructured":"Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci. 1993;90:10705\u201309.","journal-title":"Proc. Natl. Acad. Sci"},{"issue":"4","key":"276_CR26","first-page":"515","volume":"143","author":"RM Burwick","year":"2024","unstructured":"Burwick RM, Rodriguez MH. Angiogenic biomarkers in preeclampsia. J Obstet Gynaecol. 2024;143(4):515\u201323.","journal-title":"J Obstet Gynaecol"},{"issue":"3","key":"276_CR27","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1080\/10641955.2017.1329430","volume":"36","author":"JL Hecht","year":"2017","unstructured":"Hecht JL, Ordi J, Carrilho C, Ismail MR, Zsengeller ZK, Karumanchi SA, et al. The pathology of eclampsia: an autopsy series. Hypertens Pregnancy. 2017;36(3):259\u201368.","journal-title":"Hypertens Pregnancy"},{"issue":"1","key":"276_CR28","doi-asserted-by":"publisher","first-page":"100281","DOI":"10.1016\/j.clinme.2024.100281","volume":"25","author":"I Bertoni","year":"2025","unstructured":"Bertoni I, Williams S. Approach to investigation and management of proteinuria in pregnancy. Clin Med. 2025;25(1):100281.","journal-title":"Clin Med"},{"key":"276_CR29","doi-asserted-by":"crossref","unstructured":"Bartal MF, Lindheimer MD, Sibai BM. Proteinuria during pregnancy: definition, pathophysiology, methodology, and clinical significance. Am J Obstet Gynecol. 2022;S819\u201334.","DOI":"10.1016\/j.ajog.2020.08.108"},{"issue":"8","key":"276_CR30","doi-asserted-by":"publisher","first-page":"705","DOI":"10.1038\/s41371-021-00637-x","volume":"36","author":"K Chau","year":"2022","unstructured":"Chau K, Welsh M, Makris A, Hennessy A. Progress in preeclampsia: the contribution of animal models. J Hum Hypertens. 2022;36(8):705\u201310.","journal-title":"J Hum Hypertens"},{"key":"276_CR31","doi-asserted-by":"crossref","unstructured":"Bakrania BA, George EM, Granger JP. Animal models of preeclampsia: investigating pathophysiology and therapeutic targets. Am J Obstet Gynecol. 2022;226(2S):S973\u201387.","DOI":"10.1016\/j.ajog.2020.10.025"},{"key":"276_CR32","doi-asserted-by":"crossref","unstructured":"Carter AM. Animal models of human pregnancy and placentation: alternatives to the mouse. Reproduction. 2020;160(6):R129\u201343.","DOI":"10.1530\/REP-20-0354"},{"issue":"1","key":"276_CR33","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1055\/s-0041-1740939","volume":"39","author":"N Xiao","year":"2022","unstructured":"Xiao N, Lewandowski RJ. Embolic agents: coils. Semin Intervent Radiol. 2022;39(1):113\u201318.","journal-title":"Semin Intervent Radiol"},{"key":"276_CR34","doi-asserted-by":"crossref","unstructured":"Bender M, Reichart B, Figueiredo C, Burgmann JM, Leuschen M, Wall F, et al. An approach to controlling inflammation and coagulation in pig-to-baboon cardiac Xenotransplantation. Xenotransplantation. 2024;31(4):e12877.","DOI":"10.1111\/xen.12877"},{"issue":"6","key":"276_CR35","doi-asserted-by":"publisher","first-page":"596","DOI":"10.1016\/j.semnephrol.2004.07.011","volume":"24","author":"E Podjarny","year":"2004","unstructured":"Podjarny E, Losonczy G, Baylis C. Animal models of preeclampsia. Semin Nephrol. 2004;24(6):596\u2013606.","journal-title":"Semin Nephrol"},{"issue":"5","key":"276_CR36","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1177\/028418518903000514","volume":"30","author":"N Skovgaard","year":"1989","unstructured":"Skovgaard N, Holm J, Hemmingsen L, Skaarup P. Urinary protein excretion following intravenously administered ionic and non-ionic contrast media in man. Acta Radiol. 1989;30(5):517\u201319.","journal-title":"Acta Radiol"},{"key":"276_CR37","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1111\/j.1600-0684.1999.tb00085.x","volume":"28","author":"WJ Harewood","year":"1999","unstructured":"Harewood WJ, Gillin A, Hennessy A, Armistead J, Horvath JS, Tiller DJ. Biochemistry and haematology values for the baboon (Papio hamadryas): the effects of sex, growth, development and age. J Med Primarol. 1999;28:19\u201331.","journal-title":"J Med Primarol"},{"issue":"1","key":"276_CR38","doi-asserted-by":"publisher","first-page":"3018","DOI":"10.1038\/s41598-023-29651-4","volume":"13","author":"CC Colmenares-Mejia","year":"2023","unstructured":"Colmenares-Mejia CC, Quintero-Lesmes D, Bautista-Ni\u00f1o PK, Gu\u00edo E, Paez MC, Beltr\u00e1n M, et al. Uric acid and risk of pre\u2011eclampsia: results from a large case-control study and meta\u2011analysis of prospective studies. Sci Rep. 2023;13(1):3018.","journal-title":"Sci Rep"}],"container-title":["Laboratory Animal Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s42826-026-00276-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s42826-026-00276-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s42826-026-00276-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,7]],"date-time":"2026-04-07T09:17:59Z","timestamp":1775553479000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1186\/s42826-026-00276-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,7]]},"references-count":38,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["276"],"URL":"https:\/\/doi.org\/10.1186\/s42826-026-00276-8","relation":{},"ISSN":["2233-7660"],"issn-type":[{"value":"2233-7660","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,7]]},"assertion":[{"value":"11 July 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 March 2026","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 March 2026","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 April 2026","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study was approved by the Sydney Local Health District Animal Welfare Committee (protocol 2019\/001 and 2023\/003).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"Prof. Karumanchi is a co-inventor on multiple patents related to preeclampsia biomarkers and therapies that are held by the Beth Israel Deaconess Medical Center and other moieties. In addition, Prof. Karumanchi reports serving as a consultant to Aggamin Pharmaceuticals and Comanche Biopharma that are developing therapies for preeclampsia.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"12"}}