John Kingdom

Mount Sinai Hospital, Toronto, Toronto, Ontario, Canada

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Publications (230)1066.56 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: The objective of this study was to compare the in vitro contractile effects of the combination of oxytocin (low dose and high dose) with either ergonovine or carboprost in myometrial strips from women undergoing cesarean delivery (CD), and to study the effect of oxytocin pretreatment on these contractions. We hypothesized that the use of ergonovine or carboprost in combination with oxytocin would improve contractility compared with oxytocin alone. Myometrial samples obtained from women undergoing elective CD were pretreated in organ bath chambers with either oxytocin 10 M (experimental) or physiological salt solution (control) for 2 hours. They were then washed and subjected to dose-response testing with oxytocin, ergonovine, or carboprost (10 to 10 M), either alone or in combination with a fixed low-dose (10 M) (LDOx) or high-dose (10 M) (HDOx) oxytocin. The amplitude, frequency, area under the curve, and motility index (amplitude × frequency) of contractions during the dose-response period were analyzed with linear regression models, and compared among the groups. The primary outcome was the motility index across the study groups. One hundred sixty-nine experiments were done in samples obtained from 56 women. The mean square root of the motility index [standard error] (√g·contractions/10 min) of oxytocin was significantly higher in the control (3.40 [0.24]) versus experimental group (2.02 [0.15]) (P < 0.001). When all control groups were compared, the motility index of oxytocin (3.21 [0.25]) was higher than that of ergonovine (2.13 [0.30], P < 0.001 [multiple comparisons adjusted P value, P < 0.001]), carboprost (1.88 [0.10], P < 0.001 [P < 0.001]), ergonovine + LDOx (2.07 [0.15], P < 0.001 [P < 0.001]), and carboprost + LDOx (1.82 [0.15], P < 0.001 [P < 0.001]) and was not different than that of ergonovine + HDOx (3.39 [0.32], P = 0.68 [P = 0.99]) and carboprost + HDOx (2.68 [0.30], P = 0.20 [P = 0.60]). However, in oxytocin-pretreated groups, carboprost + LDOx (motility index: 2.53 [0.08], P = 0.001 [multiple comparisons adjusted P value, P = 0.002]) and ergonovine + HDOx (2.82 [0.15], P < 0.001 [P < 0.001]) exhibited significantly superior contractility response compared with oxytocin alone, while ergonovine + LDOx (2.47 [0.13], P = 0.01 [P = 0.08]) and carboprost + HDOx (2.51 [0.20], P = 0.05 [P = 0.24]) showed higher mean contractility response compared with oxytocin alone but failed to reach statistical significance in adjusted analyses. The attenuation of oxytocin-induced contractility in oxytocin-pretreated myometrial strips is in keeping with the previously established oxytocin-receptor desensitization phenomenon. Oxytocin is the most effective of the uterotonics tested if the myometrium is not preexposed to oxytocin. However, in the oxytocin-pretreated myometrium, a synergistic response is evident, and the combination of oxytocin with either ergonovine or carboprost produces superior response compared with oxytocin alone. Further in vivo studies in humans are necessary to determine whether these differences identified in vitro are clinically significant.
    Anesthesia and analgesia 03/2015; 120(5). DOI:10.1213/ANE.0000000000000682 · 3.42 Impact Factor
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    ABSTRACT: Preeclampsia (PE) increases maternal and perinatal morbidity and mortality. Based on a multitude of data from randomized clinical trials, clinical practice guidelines endorse using ASA to prevent PE in women who are "at risk." However, data are lacking about the level of absolute risk to warrant starting ASA prophylaxis. We present two approaches for objectively determining the minimum absolute risk for PE at which ASA prophylaxis is justified. The first is a new approach-the minimum control event rate (CERmin). The second approach uses a pre-existing concept-the minimum event rate for treatment (MERT). Here we show how the CERmin is derived, and then use the CERmin and the MERT to guide us to a reasonable risk threshold for starting a woman on ASA prophylaxis against PE based on clinical risk assessment. We suggest that eligible women need not be at "high risk" for preeclampsia to warrant ASA, but rather at some modestly elevated absolute risk of 6-10%. Given its very low cost, its widespread availability, ease of administration and its safety profile, ASA is a highly attractive agent for the prevention of maternal and perinatal morbidity worldwide.
    PLoS ONE 03/2015; 10(3):e0116296. DOI:10.1371/journal.pone.0116296 · 3.53 Impact Factor
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    ABSTRACT: The objective of the study was to evaluate the efficacy and safety of combined prophylactic intraoperative internal iliac artery balloon occlusion and postoperative uterine artery embolization in the conservative management (uterine preservation) of women with invasive placenta undergoing scheduled caesarean delivery. Ten women (mean age 35 years) with invasive placenta choosing caesarean delivery without hysterectomy had preoperative insertion of internal iliac artery occlusion balloons, intraoperative inflation of the balloons, and immediate postoperative uterine artery embolization with absorbable gelatin sponge. A retrospective review was performed with institutional review board approval. Outcome measures were intraoperative blood loss, transfusion requirement, hysterectomy rate, endovascular complications, surgical complications, and postoperative morbidity. All women had placenta increta or percreta, and concomitant complete placenta previa. Mean gestational age at delivery was 36 weeks. In 6 women the placenta was left undisturbed in the uterus, 2 had partial removal of the placenta, and 2 had piecemeal removal of the whole placenta. Mean estimated blood loss during caesarean delivery was 1.2 L. Only 2 patients (20%) required blood transfusion. There were no intraoperative surgical complications, endovascular complications, maternal deaths, or perinatal deaths. Three women developed postpartum complications necessitating postpartum hysterectomy; the hysterectomy rate was therefore 30% and uterine preservation was successful in 70%. Combined bilateral internal iliac artery balloon occlusion and uterine artery embolization may be an effective strategy to control intraoperative blood loss and preserve the uterus in patients with invasive placenta undergoing caesarean delivery. Copyright © 2015 Canadian Association of Radiologists. Published by Elsevier Inc. All rights reserved.
    Canadian Association of Radiologists Journal 03/2015; 66(2). DOI:10.1016/j.carj.2014.08.002 · 0.58 Impact Factor
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    ABSTRACT: -Fetal hypoxia has been implicated in the abnormal brain development seen in newborns with congenital heart disease (CHD). New magnetic resonance imaging (MRI) technology now offers the potential to investigate the relationship between fetal hemodynamics and brain dysmaturation. -We measured fetal brain size, oxygen saturation and blood flow in the major vessels of the fetal circulation in 30 late gestation fetuses with CHD and 30 normal controls using phase contrast MRI and T2 mapping. Fetal hemodynamic parameters were calculated using a combination of MRI flow and oximetry data and fetal hemoglobin concentrations estimated from population averages. In fetuses with CHD, reductions in umbilical vein oxygen content (p<0.001), and failure of the normal streaming of oxygenated blood from the placenta to the ascending aorta were associated with a mean reduction in ascending aortic saturation of 10% (p < 0.001), while cerebral blood flow and cerebral oxygen extraction were no different from controls. This accounted for the mean 15% reduction in cerebral oxygen delivery (p = 0.08) and 32% reduction cerebral VO2 in CHD fetuses (p < 0.001), which were associated with a 13% reduction in fetal brain volume (p < 0.001). Fetal brain size correlated with ascending aortic oxygen saturation and cerebral VO2 (r = 0.37 p = 0.004). -This study supports a direct link between reduced cerebral oxygenation and impaired brain growth in fetuses with CHD and raises the possibility that in utero brain development could be improved with maternal oxygen therapy.
    Circulation 03/2015; 131(15). DOI:10.1161/CIRCULATIONAHA.114.013051 · 14.95 Impact Factor
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    The Lancet 02/2015; 385(9969). DOI:10.1016/S0140-6736(15)60287-2 · 45.22 Impact Factor
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    ABSTRACT: Abstract Objectives: To determine the most reproducible method for the sonographic measurement of placental length. Methods: A prospective study of women with singleton pregnancies who underwent sonographic measurement of placental dimensions during mid-gestation. Two sonographers independently determined placental length using 3 different approaches (linear, curve-linear and panoramic) and placental thickness. Reproducibility was assessed by the Bland-Altman method and Interclass Correlation Coefficient (ICC). Results: Overall 34 women were included in the study. The curve-linear approach for the measurement of placental length was associated with the highest reproducibility (mean inter-observer difference of -0.10 cm) compared to the linear and panoramic approaches (mean difference -0.15 cm and -0.29 cm, respectively). Similarly, the ICC was highest for the curve-linear length approach (0.974) compared with the linear length and panoramic length approaches (0.956 and 0.926, respectively). Measurements of maximum placental thickness was also associated with a very good ICC (0.954). Conclusions: The curve-linear method for the measurement of placental length in the 2(nd) trimester appears to be the most reproducible approach. This technique may prove useful as an adjunct screening method, along with uterine artery Doppler and maximum placental thickness, to screen for major placental complications of pregnancy in the second trimester.
    Journal of Maternal-Fetal and Neonatal Medicine 11/2014; DOI:10.3109/14767058.2014.963047 · 1.21 Impact Factor
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    ABSTRACT: Background Thrombophilias are common disorders that increase the risk of pregnancy-associated venous thromboembolism and pregnancy loss and can also increase the risk of placenta-mediated pregnancy complications (severe pre-eclampsia, small-for-gestational-age infants, and placental abruption). We postulated that antepartum dalteparin would reduce these complications in pregnant women with thrombophilia. Methods In this open-label randomised trial undertaken in 36 tertiary care centres in five countries, we enrolled consenting pregnant women with thrombophilia at increased risk of venous thromboembolism or with previous placenta-mediated pregnancy complications. Eligible participants were randomly allocated in a 1:1 ratio to either antepartum prophylactic dose dalteparin (5000 international units once daily up to 20 weeks' gestation, and twice daily thereafter until at least 37 weeks' gestation) or to no antepartum dalteparin (control group). Randomisation was done by a web-based randomisation system, and was stratified by country and gestational age at randomisation day with a permuted block design (block sizes 4 and 8). At randomisation, site pharmacists (or delegates) received a randomisation number and treatment allocation (by fax and/or e-mail) from the central web randomisation system and then dispensed study drug to the local coordinator. Patients and study personnel were not masked to treatment assignment, but the outcome adjudicators were masked. The primary composite outcome was independently adjudicated severe or early-onset pre-eclampsia, small-for-gestational-age infant (birthweight <10th percentile), pregnancy loss, or venous thromboembolism. We did intention-to-treat and on-treatment analyses. This trial is registered with, number NCT00967382, and with Current Controlled Trials, number ISRCTN87441504. Findings Between Feb 28, 2000, and Sept 14, 2012, 292 women consented to participate and were randomly assigned to the two groups. Three women were excluded after randomisation because of ineligibility (two in the antepartum dalteparin group and one in the control group), leaving 146 women assigned to antepartum dalteparin and 143 assigned to no antepartum dalteparin. Some patients crossed over to the other group during treatment, and therefore for on-treatment and safety analysis there were 143 patients in the dalteparin group and 141 in the no dalteparin group. Dalteparin did not reduce the incidence of the primary composite outcome in both intention-to-treat analysis (dalteparin 25/146 [17·1%; 95% CI 11·4–24·2%] vs no dalteparin 27/143 [18·9%; 95% CI 12·8–26·3%]; risk difference −1·8% [95% CI −10·6% to 7·1%)) and on-treatment analysis (dalteparin 28/143 [19·6%] vs no dalteparin 24/141 [17·0%]; risk difference +2·6% [95% CI −6·4 to 11·6%]). In safety analysis, the occurrence of major bleeding did not differ between the two groups. However, minor bleeding was more common in the dalteparin group (28/143 [19·6%]) than in the no dalteparin group (13/141 [9·2%]; risk difference 10·4%, 95% CI 2·3–18·4; p=0·01). Interpretation Antepartum prophylactic dalteparin does not reduce the occurrence of venous thromboembolism, pregnancy loss, or placenta-mediated pregnancy complications in pregnant women with thrombophilia at high risk of these complications and is associated with an increased risk of minor bleeding. Funding Canadian Institutes of Health Research, Heart and Stroke Foundation of Canada, and Pharmacia and UpJohn.
    The Lancet 11/2014; 384(9955). DOI:10.1016/S0140-6736(14)60793-5 · 45.22 Impact Factor
  • Lise Huynh, John Kingdom, Sabrina Akhtar
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    ABSTRACT: To review the recent evidence behind the association of low levels (ie, below the fifth percentile) of pregnancy-associated plasma protein A (PAPP-A) with adverse perinatal outcomes and to integrate new findings with the recommendations made by the Society of Obstetricians and Gynaecologists of Canada in 2008.
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    ABSTRACT: Objective: To assess whether singleton pregnancies conceived by assisted reproductive technology (ART) are associated with an increased use of intrapartum interventions when compared with spontaneous singleton pregnancies. Methods: In total, 1327 ART pregnancies and 5222 spontaneous pregnancies during the period 2004 to 2008 were extracted from BORN (Better Outcomes Registry and Network) Ontario's information system. The incidences of common intrapartum interventions were compared, and different classification systems for Caesarean section were used to compare the indications for these between singleton pregnancies following ART with or without intracytoplasmic sperm injection and singleton spontaneously conceived pregnancies. Results: Compared with spontaneous singleton pregnancies, the ART group had increased incidences of internal electronic fetal monitoring (OR 1.60; 95% CI 1.37 to 1.87), artificial rupture of membranes (OR 1.39; 95% CI 1.17 to 1.66), oxytocin augmentation of labour (OR 1.51; 95% CI 1.28 to 1.77), induction of labour (OR 1.31; 95% CI 1.14 to 1.50), and Caesarean section (OR 1.40; 95% CI 1.24 to 1.60). Conclusion: Singleton pregnancies resulting from ART were associated with more frequent use of several intrapartum interventions, including Caesarean section.
  • Placenta 09/2014; 35(9):A76. DOI:10.1016/j.placenta.2014.06.245 · 3.29 Impact Factor
  • Anjali Kulkarni, Emily Wright, John Kingdom
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    ABSTRACT: Objective: To measure the effect of a web-based educational tool on baseline knowledge of the risks and benefits of delivery by Caesarean section in healthy nulliparous women. Methods: We constructed a web-based educational tool to provide evidence-based information on the potential benefits and risks of CS for healthy nulliparous women in the second trimester. We included women with an uncomplicated singleton pregnancy who were receiving antenatal care at Mount Sinai Hospital. Eligible women logged into the website to undertake a pre-test survey. After completing this survey, they received access to the educational tool, followed by a link to a second survey. The surveys collected baseline demographics and assessed participants' knowledge of the perceived safety and risks of vaginal delivery and CS, their sources of information, and the influence of these sources on their views. Results: Seventy-three participants completed both surveys. Participants had a high baseline preference (84%) for vaginal delivery. The mean score for knowledge about vaginal delivery and CS increased significantly between the surveys, from 47% to 76% (P < 0. 001). There was no significant change in preference for mode of delivery between the two surveys. In both surveys, more participants responded that they were a "little fearful" or "not fearful at all" of vaginal deliveries. In the second survey, significantly more responded that they were "very fearful" or "fearful" of CS (P < 0.05). Increased knowledge about specific risks of vaginal delivery did not deter participants from preferring a vaginal delivery. However, knowledge of risks associated with CS made them more likely to have "very favourable" or "somewhat favourable" views of vaginal delivery. Ethnicity and country of birth were not found to have a significant effect on preferred mode of delivery. Conclusions: We demonstrated that a web-based educational tool significantly increased knowledge of the risks and benefits of vaginal delivery and CS. However, the educational intervention did not significantly change preferences.
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    ABSTRACT: The maternal leukocytes of the first-trimester decidua play a fundamental role in implantation and early development of the fetus and placenta, yet little is known regarding the second-trimester decidual environment. Our multicolor flow cytometric analyses of human decidual leukocytes detected an elevation in tissue resident neutrophils in the second trimester. These cells in both human and murine samples were spatially restricted to decidua basalis. In comparison with peripheral blood neutrophils (PMNs), the decidual neutrophils expressed high levels of neutrophil activation markers and the angiogenesis-related proteins: vascular endothelial growth factor-A, Arginase-1, and CCL2, similarly shown in tumor-associated neutrophils. Functional in vitro assays showed that second-trimester human decidua conditioned medium stimulated transendothelial PMN invasion, upregulated VEGFA, ARG1, CCL2, and ICAM1 mRNA levels, and increased PMN-driven in vitro angiogenesis in a CXCL8-dependent manner. This study identified a novel neutrophil population with a physiological, angiogenic role in human decidua.
    The Journal of Immunology 08/2014; 193(6). DOI:10.4049/jimmunol.1303117 · 5.36 Impact Factor
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    ABSTRACT: Objective: Early identification of women at risk of developing early-onset severe preeclampsia (sPE) is a key objective in obstetrics. An elevated ratio of serum soluble fms-like tyrosine kinase (sFlt-1) to placenta-like growth factor (PlGF) (sFlt-1/PlGF ratio) precedes overt hypertension. The longitudinal relationship between this biomarker, maternal hemodynamics, and maternal serum uric acid during the pre-clinical phase is unknown. Study Design: We followed 20 normotensive women at high risk of developing sPE from 20 weeks until delivery or 34 weeks' gestation. Non-invasive hemodynamic monitoring using bioreactance technology was performed at 20 to 22, 24 to 26, 28 to 30, and 32 to 34 weeks' gestation. Serum uric acid, sFlt-1, and PlGF were measured simultaneously. Results: Six of 20 women (30%) delivered before 33 weeks with sPE and had significantly higher mean total peripheral resistance (TPR), higher serum uric acid, and higher sFlt-1/PlGF ratios at 24 weeks' gestation than unaffected individuals. The area under the curve, cut-off values, and sensitivity and specificity to predict sPE at 24 weeks were as follows: TPR 0.84, 1250, 80%, 93%; sFlt-1/PlGF ratio 0.94, 55, 100%, 93%; and serum uric acid 0.99, 255 μmol/L, 100%, 93%. TPR and sFlt-1 were positively correlated in the sPE group before antihypertensive treatment (r = 0.65, P = 0.01). Serum uric acid correlated with both sFlt-1 (r = 0.65, P = 0.003) and sFlt-1/PlGF ratio (r = 0.54, P = 0.02). Conclusion: A combination of non-invasive determination of TPR together with measurement of serum uric acid may identify a subset of clinically high-risk women with evolving sPE, independent of the determination of the sFlt-1/PlGF ratio. The predictive ability of this integrated approach needs to be assessed in a larger cohort of women to further confirm its utility.
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    ABSTRACT: To compare the in vitro contractile responses to oxytocin, ergonovine, prostaglandin F2 alpha (PGF2α), and misoprostol in isolated myometrium from non-labouring and labouring pregnant women.
    Canadian Journal of Anaesthesia 06/2014; 61(9). DOI:10.1007/s12630-014-0190-1 · 2.50 Impact Factor
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    ABSTRACT: Common pregnancy complications, such as severe preeclampsia and intrauterine growth restriction, disrupt pregnancy progression and impair maternal and fetal wellbeing. Placentas from such pregnancies exhibit lesions principally within the syncytiotrophoblast (SCT), a layer in direct contact with maternal blood. In humans and mice, glial cell missing-1 (GCM-1) promotes differentiation of underlying cytotrophoblast cells into the outer SCT layer. GCM-1 may be regulated by the transcription factor peroxisome proliferator-activated receptor-gamma (PPAR- γ ); in mice, PPAR- γ promotes labyrinthine trophoblast differentiation via Gcm-1, and, as we previously demonstrated, PPAR- γ activation ameliorates disease features in rat model of preeclampsia. Here, we aimed to characterize the baseline activity of PPAR- γ in the human choriocarcinoma BeWo cell line that mimics SCT formation in vitro and modulate PPAR- γ activity to study its effects on cell proliferation versus differentiation. We report a novel negative autoregulatory mechanism between PPAR- γ activity and expression and show that blocking PPAR- γ activity induces cell proliferation at the expense of differentiation, while these remain unaltered following treatment with the agonist rosiglitazone. Gaining a deeper understanding of the role and activity of PPAR- γ in placental physiology will offer new avenues for the development of secondary prevention and/or treatment options for placentally-mediated pregnancy complications.
    PPAR Research 02/2014; 2014:637251. DOI:10.1155/2014/637251 · 1.64 Impact Factor
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    ABSTRACT: An increasingly common challenge in antenatal care of the small for gestational age (SGA) fetus is the distinction between the constitutionally (physiologically) small fetus and the fetus affected by pathological intrauterine growth restriction (IUGR). We discuss here the rationale and the evidence for the use of customized growth percentiles for the purpose of distinguishing between the fetus with true IUGR and the fetus with constitutional SGA. We also provide estimates of the potential effects of adopting ethnicity-specific birth weight curves on the rates of SGA and large for gestational age status in multi-ethnic metropolitan cities in North America and Europe, such as the City of Toronto. Using customized growth percentiles would result in a considerable decline in the rate of a false-positive diagnosis of SGA among visible minorities, and improve the detection rate of true large for gestational age fetuses among these groups.
    Journal of obstetrics and gynaecology Canada: JOGC = Journal d'obstetrique et gynecologie du Canada: JOGC 02/2014; 36(2):164-70.
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    ABSTRACT: Preeclampsia (PE) is characterized by exaggerated apoptosis of the villous trophoblast of placental villi. Since p53 is a critical regulator of apoptosis we hypothesized that excessive apoptosis in PE is mediated by abnormal expression of proteins participating in the p53 pathway and that modulation of the p53 pathway alters trophoblast apoptosis in vitro. Fresh placental villous tissue was collected from normal pregnancies and pregnancies complicated by PE; Western blotting and real-time PCR were performed on tissue lysate for protein and mRNA expression of p53 and downstream effector proteins, p21, Bax and caspases 3 and 8. To further assess the ability of p53 to modulate apoptosis within trophoblast, BeWo cells and placental villous tissue were exposed to the p53-activator, Nutlin-3, alone or in combination with the p53-inhibitor, Pifithrin-α (PFT- α). Equally, Mdm2 was knocked-down with siRNA. Protein expression of p53, p21 and Bax was significantly increased in pregnancies complicated by PE. Conversely, Mdm2 protein levels were significantly depleted in PE; immunohistochemistry showed these changes to be confined to trophoblast. Reduction in the negative feedback of p53 by Mdm2, using siRNA and Nutlin-3, caused an imbalance between p53 and Mdm2 that triggered apoptosis in term villous explants. In the case of Nutlin, this was attenuated by Pifithrin-α. These data illustrate the potential for an imbalance in p53 and Mdm2 expression to promote excessive apoptosis in villous trophoblast. The upstream regulation of p53 and Mdm2, with regard to exaggerated apoptosis and autophagy in PE, merits further investigation.
    PLoS ONE 01/2014; 9(1):e87621. DOI:10.1371/journal.pone.0087621 · 3.53 Impact Factor
  • American Journal of Obstetrics and Gynecology 01/2014; 210(1):S311. DOI:10.1016/j.ajog.2013.10.667 · 3.97 Impact Factor

Publication Stats

6k Citations
1,066.56 Total Impact Points


  • 1999–2015
    • Mount Sinai Hospital, Toronto
      • • Department of Obstetrics and Gynecology
      • • Department of Anesthesia
      • • Department of Fetal Medicine
      Toronto, Ontario, Canada
  • 1998–2015
    • University of Toronto
      • • Department of Obstetrics and Gynaecology
      • • Mount Sinai Hospital
      Toronto, Ontario, Canada
  • 1998–2014
    • Samuel Lunenfeld Research Institute
      Toronto, Ontario, Canada
  • 2010–2011
    • SickKids
      • Division of Rheumatology
      Toronto, Ontario, Canada
  • 2004–2011
    • Mount Sinai Hospital
      New York City, New York, United States
  • 2001–2011
    • Sinai Hospital
      Mount Sinai, New York, United States
    • RWTH Aachen University
      Aachen, North Rhine-Westphalia, Germany
  • 2009
    • Shanghai Jiao Tong University
      Shanghai, Shanghai Shi, China
  • 2006
    • Leiden University Medical Centre
      • Department of Obstetrics
      Leiden, South Holland, Netherlands
  • 2005
    • University College London Hospitals NHS Foundation Trust
      Londinium, England, United Kingdom
  • 2000
    • Queen's University
      • Department of Obstetrics and Gynaecology
      Kingston, Ontario, Canada
    • The Fetal Medicine Foundation
      Londinium, England, United Kingdom
  • 1993–1999
    • University of Glasgow
      Glasgow, Scotland, United Kingdom
  • 1997
    • University College London
      Londinium, England, United Kingdom
  • 1996
    • Justus-Liebig-Universität Gießen
      • Institut für Veterinär-Anatomie, -Histologie und -Embryologie
      Gießen, Hesse, Germany
  • 1994
    • WWF United Kingdom
      Londinium, England, United Kingdom
    • University of Birmingham
      Birmingham, England, United Kingdom
  • 1991
    • The Queen's Medical Center
      Honolulu, Hawaii, United States
  • 1990
    • Medical Research Council (UK)
      Londinium, England, United Kingdom