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F. Foo, A. Mahendru, G. Masini, A. Fraser, Stefano Cacciatore, D. MacIntyre, C. McEniery, I. Wilkinson, P. Bennett, C. Lees (2018)Association Between Prepregnancy Cardiovascular Function and Subsequent Preeclampsia or Fetal Growth Restriction
F. Versen-Höynck, F. Versen-Höynck, A. Schaub, Yueh-Yun Chi, Kuei-Hsun Chiu, Jing Liu, M. Lingis, R. Williams, A. Rhoton-Vlasak, W. Nichols, Raquel Fleischmann, Wendy Zhang, V. Winn, M. Segal, K. Conrad, V. Baker (2019)Increased Preeclampsia Risk and Reduced Aortic Compliance With In Vitro Fertilization Cycles in the Absence of a Corpus Luteum
E. Magnussen, L. Vatten, T. Lund-Nilsen, K. Salvesen, G. Smith, P. Romundstad (2007)Prepregnancy cardiovascular risk factors as predictors of pre-eclampsia: population based cohort study
BMJ : British Medical Journal, 335
E. Fujitake, R. Jaspal, L. Monasta, T. Stampalija, C. Lees (2020)Acute cardiovascular changes in women undergoing in vitro fertilisation (IVF), a systematic review and meta-analysis.
European journal of obstetrics, gynecology, and reproductive biology, 248
J. Tay, L. Foo, G. Masini, P. Bennett, C. McEniery, I. Wilkinson, C. Lees (2018)Early and late preeclampsia are characterized by high cardiac output, but in the presence of fetal growth restriction, cardiac output is low: insights from a prospective study
American Journal of Obstetrics and Gynecology, 218
Xiao-Ling Hu, Chun Feng, Xianhua Lin, Zi-Xing Zhong, Yi-Min Zhu, P. Lv, M. Lv, Y. Meng, Dan Zhang, X. Lu, F. Jin, J. Sheng, Jian Xu, He-feng Huang (2014)High maternal serum estradiol environment in the first trimester is associated with the increased risk of small-for-gestational-age birth.
The Journal of clinical endocrinology and metabolism, 99 6
M. Leitman, E. Sucher, E. Kaluski, R. Wolf, E. Peleg, Y. Moshkovitz, O. Milo-Cotter, Z. Vered, G. Cotter (2006)Non‐invasive measurement of cardiac output by whole‐body bio‐impedance during dobutamine stress echocardiography: Clinical implications in patients with left ventricular dysfunction and ischaemia
European Journal of Heart Failure, 8
J. Saur, F. Trinkmann, C. Doesch, Joerg Weissmann, K. Hamm, Stefan Schoenberg, Martin Borggrefe, D. Haghi, J. Kaden (2010)Non-Invasive Measurement of Cardiac Output during Atrial Fibrillation: Comparison between Cardiac Magnetic Resonance Imaging and Inert Gas Rebreathing
Kirk Conrad, John Petersen, Yueh-Yun Chi, Xiao-mei Zhai, Minjie Li, Kuei-Hsun Chiu, Jing Liu, M. Lingis, R. Williams, A. Rhoton-Vlasak, Joseph Larocca, Wilmer Nichols, Mark Segal (2019)Maternal Cardiovascular Dysregulation During Early Pregnancy After In Vitro Fertilization Cycles in the Absence of a Corpus Luteum.
P. Peyton, B. Thompson (2004)Agreement of an Inert Gas Rebreathing Device with Thermodilution and the Direct Oxygen Fick Method in Measurement of Pulmonary Blood Flow
Journal of Clinical Monitoring and Computing, 18
L. Critchley, Anna Lee, A. Ho (2010)A Critical Review of the Ability of Continuous Cardiac Output Monitors to Measure Trends in Cardiac Output
Anesthesia & Analgesia, 111
Background: Haemodynamic assessment in and before pregnancy is becoming increasingly important in relation to pregnancy complications and outcomes. Different methodologies exist but there is no gold‑standard technique for non‑invasive measurement of cardiac output (CO). We sought to assess two methods of CO measurement in healthy women undergoing in vitro fertilisation cycles (IVF). This was a prospective longitudinal study of 71 women aged 18–44 years planning IVF undergoing CO measurements obtained via inert gas rebreathing (IGR) using I nnocor and whole‑body bio ‑impedance ( WBI) using Nicas to assess the reproducibility between the methods. Four visits occurred at which both techniques were used: initial assessment, embryo transfer, day of pregnancy test and 4 weeks post‑transfer (regardless of whether conception occurred). Cross‑sectional agreement of the methods was assessed using the calculation of bias, percentage error and limits of agreement (LOA) via the Bland–Altman analysis. Longitu‑ dinal agreement of the methods was assessed using a 4‑ quadrant plot with concordance rate, angular bias and radial limits of agreement (%). Results: One hundred and thirteen measurements from 44 participants were suitable for cross‑sectional (Bland–Alt ‑ ™ ™ man) analysis. IGR (Innocor ) Mean CO was 4.61 L/min and 5.05 L/min with WBI (N icas ). The bias was 0.44 L/min. The percentage error was 76% and intra‑ correlation coefficient was 0.135 (95% CI −0.43–0.306). Fifty‑nine measurements from 28 participants were suitable for longitudinal (4Q‑plot) analysis. The concordance rate was 64.4%, angular bias – 0.14, and radial limits of agreement + − 13.25°. Conclusion: There was poor cross‑sectional and longitudinal agreement between inert gas rebreathing and whole ‑ body bio‑impedance techniques. These techniques cannot be used interchangeably when measuring CO in women undergoing IVF, and these results may be more generalizable, to women in the peri‑ conception period. Keywords: Cardiovascular, Maternal haemodynamics, Non‑invasive, Assisted reproductive techniques, In vitro fertilisation 1 Background *Correspondence: firstname.lastname@example.org Disordered cardiovascular adaptation in pregnancy is associated with pre-eclampsia and growth-restricted Centre for Fetal Care, Queen Charlotte’s and Chelsea Hospital, Du Cane Rd, London W12 0HS, UK babies . The known acute effects of IVF on maternal Full list of author information is available at the end of the article © The Author(s) 2022, corrected publication 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Jaspal et al. Artery Research (2022) 28:100–104 101 haemodynamics are limited  and no gold-standard 3 Methods method for non-invasively measuring CO in this pop- We conducted a prospective longitudinal cohort study, ulation exists. In fresh IVF cycles, ovarian stimula- recruiting healthy women aged 18–44 years between tion leads to acutely supra-physiological oestradiol , 23rd September 2018 and 4th December 2019, plan- not experienced in spontaneous conception. Frozen ning to undergo IVF. By virtue of UK NHS IVF funding embryo replacement cycles (FET) require no ovarian criteria, all had a BMI under 30 and were non-smokers. stimulation and have no corpus lutea, which has been Women underwent fresh (ovarian stimulation) cycles and associated with cardiovascular maladaptation and frozen embryo replacement cycles (FET). The study pro - increased pre-eclampsia risk in FET conceived preg- tocol is summarised in Fig. 1. nancies [4, 5]. Women were recruited via one inner city fertility clinic Invasive methods of measuring CO are unacceptable and gave written consent. Exclusion criteria were: pre- in healthy women trying to conceive. Innocor (Inno- existing chronic medical co-morbidity, including cardio- vision, Denmark) uses inert gas rebreathing (IGR) to vascular disease. calculate CO and compares well to cardiac MRI . Four study visits occurred (Fig. 1), prior and post- Nicas (Niccom, Israel), utilises whole-body bio- embryo transfer. impedance (WBI) and compares favourably with Dop- At each visit, cardiac output was assessed non-inva- pler echo, with a correlation of (R) 0.81 . sively via inert gas rebreathing (IGR) using the Innocor , and whole-body bio-impedance (WBI) using the Nicas , consecutively in that order. IGR was taken as the refer- 2 Aim ence technique as the more established method which To compare the whole-body impedance (WBI) Nicas has compared favourably with invasive methods and car- method to the inert gas rebreathing Inno cor method diac magnetic resonance imaging (MRI) [6, 8]. of evaluating cardiac output in women undergoing The process and sequence of measurements were the in vitro fertilisation. same for every study visit and patients were refrained Fig. 1 Cardiovascular changes during assisted reproductive techniques study protocol. FET = frozen embryo transfer BMI = body mass index SV = stroke volume CO = cardiac output Jaspal et al. Artery Research (2022) 28:100–104 102 from caffeinated drinks and strenuous exercise for at 6 Results least two hours prior to the visit. Patients were acclima- Seventy-one patients were recruited over a 1-year period tised in a temperature-controlled room for 10 min prior (September 2018–December 2019). Thirty-four patients to measurements being recorded. underwent frozen cycles (FET) and 39 had fresh cycles. Data were analysed using IBM SPSS Version 24.0 Baseline demographics for all participants are shown in Table 1. 4 Cross‑sectional Analysis Cross-sectional analysis required paired measurements Absolute values of simultaneous CO measurements from both devices at the same time point, therefore, a with both techniques obtained at each visit were used total of 113 paired measurements taken from 44 partici- for comparison. There was no correction for repeated pants were suitable for Bland–Altman analysis. A visual measurements within subjects between visits. Agree- representation of the agreement in CO measurements ment was assessed using Bland–Altman (BA) plots and between the two devices was constructed using a Bland– statistics and intraclass correlation. BA statistics included Altman plot; see Fig. 2. Mean CO was 4.61 L/min and ™ ™ mean CO, bias (reflecting accuracy), limits of agreement 5.05 L/min for Innocor and Nicas , respectively. The and percentage error (reflecting precision). Good agree - bias was 0.44 L/min and the LOA were 3.24 to − 4.12. ment was considered with a low bias (< 0.75 L/min), The percentage error was 76%. The ICC was 0.135 (95% percentage error < 30% and intra-correlation coefficient CI − 0.43–0.306). (ICC) > 0.75 L/min. Longitudinal analysis required paired measurements from both devices across incremental visits; therefore, 59 5 Longitudinal Analysis measurements from 28 participants were suitable for the Trending capacity of both techniques was compared 4-quadrant plot; see Fig. 3. using 4-quadrant plot a concordance analysis. Differ - Concordant results, i.e. where the devices detect a ences in cardiac output (ΔCO) between 2 consecutive change in CO in the same direction are demonstrated in visits (1–2, 2–3, 3–4 and 1–4) were compared between the upper right and lower left quadrants. Non-concord- both techniques. An exclusion zone of 0.5 L/min was ant results, i.e. where the devices detect a change in CO considered. Concordance was calculated along with in opposite directions are represented by data points in angular bias and radial limits of agreement. Acceptable the upper left and lower right quadrants. The concord - agreement was to be defined as a concordance rate > 90% ance rate between the devices was 64.4%, angular bias with angular bias < 5° and RAL + – 30° . was − 0.14°, and radial limits of agreement + − 13.25%. Table 1 Demographic data All participants Participants included in cross- Participants included in sectional comparison of CO longitudinal comparison of CO Participants (n) 71 44 28 Mean maternal age—years (SD) 35.03 (4.08) 34.82 (3.75) 35.43 (3.39) Caucasian, n (%) 34 (47.9) 23 (51.1) 14 (50) Asian, n (%) 20 (28.2) 11 (24.4) 5 (17.9) Black, n (%) 7 (9.86) 6 (13.3) 5 (17.9) Other ethnicity, n (%) 10 (13.2) 5 (11.1) 4 (14.3) Mean alcohol intake‑units (SD) 1.7 (2.63) 1.75 (2.90) 2.04 (3.25) Mean caffeine intake ‑ cups/day (SD) 1.46 (1.52) 1.51 (1.56) 1.5 (1.64) Smokers, n (%) 13 (17.1) 9 (20) 6 (21.4) Mean body mass index (SD) 24.76 (3.66) 24.87 (3.39) 25.12 (3.28) Mean body surface area‑m (SD) 1.72 (0.15) 1.73 (0.16) 1.73 (0.16) All participants and further specified for those used in the Bland–Altman and longitudinal analysis CO cardiac output, SD standard deviation Jaspal et al. Artery Research (2022) 28:100–104 103 ™ ™ Fig. 2 The Bland–Altman Analysis, a cross‑sectional analysis of measurements of CO taken with Nicas compared to Innocor ™ ™ Fig. 3 4‑ quadrant plot; the change in CO (L/min) between visits using Innocor and Nicas . The red box represents the exclusion zone of 10% (0.5 L/min) and the red diagonal line represents CO Jaspal et al. Artery Research (2022) 28:100–104 104 Declarations 7 Discussion There is emerging interest in assessing cardiac output Conflict of Interest and other cardiovascular parameters, cross-sectionally The authors declare that they have no competing interests. and longitudinally prior and during pregnancy. There is Ethical Approval evidence that blood pressure prior to pregnancy is asso- Granted by Cambridge East NEC in August 2018. ciated with risk of pre-eclampsia  and low cardiac Consent for Publication output prior to pregnancy in healthy women is associ- Not applicable. ated with the development of pre-eclampsia or growth- restricted babies . In addition to these considerations, Author details Centre for Fetal Care, Queen Charlotte’s and Chelsea Hospital, Du Cane Rd, the supra-physiological doses of hormonal drugs used in London W12 0HS, UK. Imperial College London, South Kensington, London, IVF may have a profound effect on the maternal cardio - UK. Erasmus Medical Centre, Rotterdam, The Netherlands. vascular system, albeit for a short time. Received: 28 April 2022 Accepted: 4 July 2022 In this, the only study of its type, we compared a rela- Published online: 3 August 2022 tively newer method of WBI to IGR, which has been favourably compared to other methods such as cardiac MRI . A large number of paired readings were used ™ ™ References to compare IGR using Inno cor and WBI using Nic as 1. Tay J, Foo L, Masini G, Bennett PR, McEniery CM, Wilkinson IB, et al. Early cross-sectionally and longitudinally. Bias (0.44 L/min) and late preeclampsia are characterized by high cardiac output, but in was within accepted limits which demonstrates reasona- the presence of fetal growth restriction, cardiac output is low: insights from a prospective study. Am J Obstet Gynecol. 2018;218(5):517. ble accuracy but a wide LOA and PE of 76% and low ICC 2. Fujitake E, Jaspal R, Monasta L, Stampalija T, Lees C. Acute cardio‑ shows limited precision and, therefore, poor agreement vascular changes in women undergoing in vitro fertilisation (IVF), a between both the methods. systematic review and meta‑analysis. Eur J Obstet Gynecol Reprod Biol. 2020;248:245–51. Comparison of trending capacities of both devices 3. Hu XL, Feng C, Lin XH, Zhong ZX, Zhu YM, Lv PP, et al. High maternal showed a concordance rate (76%) far below the generally serum estradiol environment in the first trimester is associated with the accepted 90% level for good agreement. increased risk of small‑for ‑ gestational‑age birth. J Clin Endocrinol Metab. 2014;99(6):2217–24. To our knowledge, this is the only study comparing 4. Conrad KP, Petersen JW, Chi YY, Zhai X, Li M, Chiu KH, et al. Maternal the two techniques, and has a large number of measure- cardiovascular dysregulation during early pregnancy after in vitro ments, making the findings robust. In conclusion, it is not fertilization cycles in the absence of a corpus luteum. Hypertension. 2019;74(3):705–15. possible to use these non-invasive methods interchangea- 5. von Versen‑Hoynck F, Schaub AM, Chi YY, Chiu KH, Liu J, Lingis M, et al. bly, for absolute measurements or for trend analysis with Increased preeclampsia risk and reduced aortic compliance with in vitro time as agreement for both absolute CO measurements fertilization cycles in the absence of a corpus luteum. Hypertension. 2019;73(3):640–9. and tracking changes in CO between these techniques is 6. FT JS, Doesch C, Weissman J, Hamm K, Schoenberg SO, Borggrefe M, limited. Haghi D, Kaden JJ. Non‑invasive measurement of cardiac output during atrial fibrillation: comparison between cardiac magnetic resonance imag‑ ing and inert gas rebreathing. Cardiology. 2010;115:212–6. Abbreviations 7. Leitman M, Sucher E, Kaluski E, Wolf R, Peleg E, Moshkovitz Y, et al. Non‑ BA: Bland–Altman; BMI: Body mass index; CO: Cardiac output; FET: Frozen invasive measurement of cardiac output by whole‑body bio ‑impedance embryo transfer; ICC: Intra‑ correlation coefficient; IGR: Inert gas rebreathing; during dobutamine stress echocardiography: clinical implications in IVF: In vitro fertilisation; LOA: Limits of agreement; SD: Standard deviation; SV: patients with left ventricular dysfunction and ischaemia. Eur J Heart Fail. Stroke volume; WBI: Whole‑body bio ‑impedance. 2006;8(2):136–40. 8. Peyton PJ, Thompson B. Agreement of an inert gas rebreathing device Acknowledgements with thermodilution and the direct oxygen Fick method in measurement Research Midwives Olive Adams and Jenny Harding who were instrumental to of pulmonary blood flow. J Clin Monit Comput. 2004;18(5–6):373–8. patient recruitment and data collection. 9. Critchley LA, Lee A, Ho AM. A critical review of the ability of continuous cardiac output monitors to measure trends in cardiac output. Anesth Author Contributions Analg. 2010;111(5):1180–92. The authors RJ and CL wrote the study protocol and submitted and obtained 10. Magnussen EB, Vatten LJ, Lund‑Nilsen TI, Salvesen KA, Davey Smith G, ethical approval. RJ and MA carried out patient recruitment, data collection Romundstad PR. Prepregnancy cardiovascular risk factors as predictors of and interpretation. DR and JC performed the statistical analysis. RJ and MA pre‑ eclampsia: population based cohort study. BMJ. 2007;335(7627):978. wrote the paper with the supervision of CL and input from DR and JC. 11. Foo FL, Mahendru AA, Masini G, Fraser A, Cacciatore S, MacIntyre DA, et al. Association between prepregnancy cardiovascular function and Funding subsequent preeclampsia or fetal growth restriction. Hypertension. Imperial College Health Charity Cardiovascular Grant. No involvement in study 2018;72(2):442–50. design, data collection, analysis or interpretation. Funding for study consuma‑ bles only. CCL is supported by the NIHR Biomedical Research Centre (BRC) based at Imperial College Healthcare NHS Trust and Imperial College London. Availability of Data and Materials The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Artery Research – Springer Journals
Published: Sep 1, 2022
Keywords: Cardiovascular; Maternal haemodynamics; Non-invasive; Assisted reproductive techniques; In vitro fertilisation
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