Disaccharide compositional analysis of chondroitin sulphate using WAX HILIC-MS with pre-column procainamide labelling; application to the placenta in pre-eclampsia

Article

Antia, I., Hills, F. and Shah, A. 2024. Disaccharide compositional analysis of chondroitin sulphate using WAX HILIC-MS with pre-column procainamide labelling; application to the placenta in pre-eclampsia. Analytical Methods. 16 (4), pp. 566-575. https://doi.org/10.1039/D3AY01578E
TypeArticle
TitleDisaccharide compositional analysis of chondroitin sulphate using WAX HILIC-MS with pre-column procainamide labelling; application to the placenta in pre-eclampsia
AuthorsAntia, I., Hills, F. and Shah, A.
Abstract

Chondroitin sulphate (CS) and dermatan sulphate are linear negatively charged heteropolysaccharides. These glycosaminoglycans are involved in cellular signalling via binding to growth factors. CS is expressed in a range of tissue and biological fluids and is highly expressed in the placenta. There is evidence that decorin; a CS proteoglycan is significantly decreased in pre-eclampsia and fetal growth restriction. It is considered that GAG chain composition may influence cellular processes that are altered in pre-eclampsia. The goal of the present study was to develop an LC-MS method with precolumn procainamide labelling for the disaccharide compositional analysis of CS. The method was used to investigate whether the disaccharide composition of placenta-extracted CS is altered in pre-eclampsia. The study revealed differential disaccharide compositions of placental chondroitin sulphate disaccharide between pre-eclampsia and other pregnancy samples. This suggests that the method may have diagnostic potential for pregnancy disorders. Furthermore, the findings suggest that CS sulphation might play a significant role in maternal labour.

KeywordsChondroitin sulphate; dermatan sulphate; pregnancy disorders; LC-MS; procainamide
Sustainable Development Goals3 Good health and well-being
Middlesex University ThemeHealth & Wellbeing
Research GroupReproductive Biology group
PublisherRoyal Society of Chemistry (RSC)
JournalAnalytical Methods
ISSN1759-9660
Electronic1759-9679
Publication dates
Online08 Jan 2024
Print25 Jan 2024
Publication process dates
Submitted06 Sep 2023
Accepted17 Dec 2023
Deposited11 Jan 2024
Output statusPublished
Accepted author manuscript
File Access Level
Open
Supplemental file
File Access Level
Open
Digital Object Identifier (DOI)https://doi.org/10.1039/D3AY01578E
PubMed ID38189556
Web of Science identifierWOS:001142097600001
LanguageEnglish
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Heidbreder, C., Foxton, R., Cilia, J., Hughes, Z., Shah, A., Atkins, A., Hunter, J., Hagan, J. and Jones, D. 2001. Increased responsiveness of dopamine to atypical, but not typical antipsychotics in the medial prefrontal cortex of rats reared in isolation. Psychopharmacology. 156 (2-3), pp. 338-351. https://doi.org/10.1007/s002130100760
Development of a high-pressure gradient pumping system for parallel liquid chromatography/mass spectrometry for the analysis of combinatorial libraries
Tolson, D., Organ, A. and Shah, A. 2001. Development of a high-pressure gradient pumping system for parallel liquid chromatography/mass spectrometry for the analysis of combinatorial libraries. Rapid Communications in Mass Spectrometry. 15 (14), pp. 1244-1249. https://doi.org/10.1002/rcm.359
The evaluation of interdigitated array electrodes for the measurement of catecholamines and indoleamines
Senior, J., Shah, A., Monteux, C. and de Biasi, V. 2001. The evaluation of interdigitated array electrodes for the measurement of catecholamines and indoleamines. Journal of Pharmaceutical and Biomedical Analysis. 24 (5-6), pp. 843-848. https://doi.org/10.1016/S0731-7085(00)00551-3
Development and application of a sensitive high performance ion-exchange chromatography method for the simultaneous measurement of dopamine, 5-hydroxytryptamine and norepinephrine in microdialysates from the rat brain
Heidbreder, C., Lacroix, L., Atkins, A., Organ, A., Murray, S., West, A. and Shah, A. 2001. Development and application of a sensitive high performance ion-exchange chromatography method for the simultaneous measurement of dopamine, 5-hydroxytryptamine and norepinephrine in microdialysates from the rat brain. Journal of Neuroscience Methods. 112 (2), pp. 135-144. https://doi.org/10.1016/S0165-0270(01)00460-5
Determination of β-lactams and their biosynthetic intermediates in fermentation media by pre-column derivatisation followed by fluorescence detection
Shah, A. and Adlard, M. 1988. Determination of β-lactams and their biosynthetic intermediates in fermentation media by pre-column derivatisation followed by fluorescence detection. Journal of Chromatography B: Biomedical Sciences and Applications. 424, pp. 325-336. https://doi.org/10.1016/S0378-4347(00)81109-3
Evaluation of expression and function of the H+/myo-inositol transporter HMIT;
Di Daniel, E., Mok, S., Mead, E., Mutinelli, C., Zambello, E., Caberlotto, L., Pell, T., Langmead, C., Shah, A., Duddy, G., Kew, J. and Maycox, P. 2009. Evaluation of expression and function of the H+/myo-inositol transporter HMIT; BMC Cell Biology. 10. https://doi.org/10.1186/1471-2121-10-54
Elucidating the intra-species proteotypes of pseudomonas aeruginosa from cystic fibrosis
Olkun, A., Shah, A. and Shah, H. 2017. Elucidating the intra-species proteotypes of pseudomonas aeruginosa from cystic fibrosis. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford, UK Wiley. pp. 579-592
Subtyping of Staphylococcus spp. Based upon MALDI-TOF MS data analysis
Xu, Z., Olkun, A., Vranckx, K., Mkrtchyan, H., Shah, A., Pot, B., Cutler, R. and Shah, H. 2017. Subtyping of Staphylococcus spp. Based upon MALDI-TOF MS data analysis. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford, UK Wiley. pp. 563-578
Determination of antimicrobial resistance using tandem mass spectrometry
Shah, A., Serafim, V., Xu, Z., Mkrtchyan, H. and Shah, H. 2017. Determination of antimicrobial resistance using tandem mass spectrometry. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford, UK Wiley. pp. 399-418
Microbial DNA analysis by MALDI-TOF mass spectrometry
Honisch, C., Serafim, V., Hennessy, N., Allen, D., Ring, C., Pantoja Munoz, L., Gharbia, S., Shah, A. and Shah, H. 2017. Microbial DNA analysis by MALDI-TOF mass spectrometry. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford Wiley. pp. 187-209
Competition intensity and fatigue in elite fencing
Turner, A., Kilduff, L., Mrashall, G., Phillips, J., Noto, A., Buttigeig, C., Gondek, M., Hills, F. and Dimitriou, L. 2017. Competition intensity and fatigue in elite fencing. The Journal of Strength and Conditioning Research. 31 (11), pp. 3128-3136. https://doi.org/10.1519/JSC.0000000000001758
Detection and quantification of human chorionic gonadotropin levels in human placental choriocarcinoma cell lines
Gondek, M., Hills, F. and Burczynska, B. 2017. Detection and quantification of human chorionic gonadotropin levels in human placental choriocarcinoma cell lines. 2017 Middlesex University Postgraduate Researchers Summer Conference. Middlesex University London, UK 28 - 29 Jun 2017
The effect of plasma volume on changes in biomarkers of muscle damage, inflammation, oxidative stress and leukocyte differentialfollowing a 42.2 km trail run, and the efficacy of recovery interventions
Cockburn, E., Hills, F., Wilson, L., Paice, K., Wood, A. and Dimitriou, L. 2017. The effect of plasma volume on changes in biomarkers of muscle damage, inflammation, oxidative stress and leukocyte differentialfollowing a 42.2 km trail run, and the efficacy of recovery interventions. BASES-FEPSAC Conference 2017. Nottingham, UK 28 - 29 Nov 2017 Taylor & Francis (Routledge). pp. s26
Influence of cold water immersion and cherry juice on recovery following a 42.2km trail run
Paice, K., Dimitriou, L., Wilson, L., Hills, F., Sinclair, S., Gondek, M., Kwan Xue Bin, X., Wood, A. and Cockburn, E. 2017. Influence of cold water immersion and cherry juice on recovery following a 42.2km trail run. BASES-FEPSAC Conference 2017. Nottingham, UK 28 - 29 Nov 2017 Taylor & Francis (Routledge). pp. s92
Fitness analysis of tetracycline resistant and sensitive Shigella flexneri in lethal and sub-lethal concentrations of tetracycline in Thames river water microcosms
Maruzani, R., Shah, A., Pantoja Munoz, L. and Marvasi, M. 2017. Fitness analysis of tetracycline resistant and sensitive Shigella flexneri in lethal and sub-lethal concentrations of tetracycline in Thames river water microcosms. 2017 Middlesex University Postgraduate Researchers Summer Conference. Middlesex University London, UK 28 - 29 Jun 2017
The influence of cold water immersion on markers of recovery following resistance exercise
Wilson, L., Dimitriou, L., Hills, F., Gondek, M. and Cockburn, E. 2017. The influence of cold water immersion on markers of recovery following resistance exercise. BASES-FEPSAC Conference 2017. Nottingham, UK 28 - 29 Nov 2017 Taylor & Francis (Routledge). pp. s66
Classification of cancer cell lines using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and statistical analysis
Serafim, V., Shah, A., Puiu, M., Andreescu, N., Coricovac, D., Nosyrev, A., Spandidos, D., Tsatsakis, A., Dehelean, C. and Pinzaru, I. 2017. Classification of cancer cell lines using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and statistical analysis. International Journal of Molecular Medicine. 40 (4), pp. 1096-1104. https://doi.org/10.3892/ijmm.2017.3083
Rapid identification of E. coli bacteriophages using mass spectrometry
Serafim, V., Ring, C., Pantoja Munoz, L., Shah, H. and Shah, A. 2017. Rapid identification of E. coli bacteriophages using mass spectrometry. Journal of Proteomics and Enzymology. 6 (1), pp. 1-5. https://doi.org/10.4172/2470-1289.1000130
Heparan sulfate disaccharide measurement from biological samples using pre-column derivatization, UPLC-MS and single ion monitoring
Antia, I., Yagnik, D., Pantoja Munoz, L., Shah, A. and Hills, F. 2017. Heparan sulfate disaccharide measurement from biological samples using pre-column derivatization, UPLC-MS and single ion monitoring. Analytical Biochemistry. 530, pp. 17-30. https://doi.org/10.1016/j.ab.2017.04.019
Detection of the tau protein in human serum by a sensitive four-electrode electrochemical biosensor
Wang, S., Acha, D., Shah, A., Hills, F., Roitt, I., Demosthenous, A. and Bayford, R. 2017. Detection of the tau protein in human serum by a sensitive four-electrode electrochemical biosensor. Biosensors and Bioelectronics. 92, pp. 482-488. https://doi.org/10.1016/j.bios.2016.10.077
Can you spot the difference? Analysis of human chorionic gonadotropin (hCG) secreted by common non-trophoblastic and trophoblastic cancers
Gondek, M., Hills, F. and Burczynska, B. 2015. Can you spot the difference? Analysis of human chorionic gonadotropin (hCG) secreted by common non-trophoblastic and trophoblastic cancers. 2015 Middlesex University Postgraduate Researchers Summer Conference. Middlesex University London, UK 17 - 18 Jun 2015 Middlesex University.
Determination of urinary cortisol, cortisone and 6-sulfatoxymelatonin using dilute and shoot ultra-high pressure liquid chromatography-tandem mass spectrometry
Sniecinska-Cooper, A., Shah, A., Dimitriou, D., Iles, R., Butler, S. and Bayford, R. 2015. Determination of urinary cortisol, cortisone and 6-sulfatoxymelatonin using dilute and shoot ultra-high pressure liquid chromatography-tandem mass spectrometry. Journal of Chromatography B. 978-79, pp. 18-23. https://doi.org/10.1016/j.jchromb.2014.11.016
The role of vitamin In type 2 diabetes
Ali, A., Appiah, S., Shah, A. and Ghali, L. 2014. The role of vitamin In type 2 diabetes. 2014 Middlesex University Postgraduate Researchers Summer Conference. Middlesex University London, UK 19 Jun 2014
Placental syndecan-1 and sulphated glycosaminoglycans are decreased in preeclampsia
Heyer-Chauhan, N., Ovbude, I., Hills, A., Sullivan, M. and Hills, F. 2013. Placental syndecan-1 and sulphated glycosaminoglycans are decreased in preeclampsia. Journal of Perinatal Medicine. https://doi.org/10.1515/jpm-2013-0097
IGFBP-1 in the placenta, membranes and fetal circulation: levels at term and preterm delivery
Hills, F., Gunn, L., Hardiman, P., Thanaratnam, S. and Chard, T. 1996. IGFBP-1 in the placenta, membranes and fetal circulation: levels at term and preterm delivery. Early Human Development. 44 (1), pp. 71-76.
Effects of N-acetylaspartylglutamate (NAAG) at group II mGluRs and NMDAR
Fricker, A., Mok, M., De la Flor, R., Shah, A., Woolley, M., Dawson, L. and Kew, J. 2009. Effects of N-acetylaspartylglutamate (NAAG) at group II mGluRs and NMDAR. Neuropharmacology. 56 (6-7), pp. 1060-1067. https://doi.org/10.1016/j.neuropharm.2009.03.002
Development and application of a liquid chromatography/tandem mass spectrometric assay for measurement of N-acetylaspartate, N-acetylaspartylglutamate and glutamate in brain slice superfusates and tissue extracts
Shah, A., De la Flor, R., Atkins, A., Slone-Murphy, J. and Dawson, L. 2008. Development and application of a liquid chromatography/tandem mass spectrometric assay for measurement of N-acetylaspartate, N-acetylaspartylglutamate and glutamate in brain slice superfusates and tissue extracts. Journal of Chromatography B. 876 (2), pp. 153-158. https://doi.org/10.1016/j.jchromb.2008.10.012
Development of Zwitterionic Hydrophilic Liquid Chromatography (ZICⓇHILIC-MS) metabolomics method for Shotgun analysis of human urine
Trivedi, D., Jones, H., Shah, A. and Iles, R. 2012. Development of Zwitterionic Hydrophilic Liquid Chromatography (ZICⓇHILIC-MS) metabolomics method for Shotgun analysis of human urine. Journal of Chromatography & Separation Techniques. 03 (06). https://doi.org/10.4172/2157-7064.1000144
Differential proteolysis of insulin-like growth factor binding protein-1 (IGFBP-1) in pregnancy
Hills, F., Iles, R. and Sullivan, M. 2013. Differential proteolysis of insulin-like growth factor binding protein-1 (IGFBP-1) in pregnancy. Journal of Perinatal Medicine. 41 (3), pp. 241-249. https://doi.org/10.1515/jpm-2012-0086
A high-performance liquid chromatography/tandem mass spectrometry assay for the simultaneous measurement of acetylcholine and clozapine in microdialysis samples
Shah, A. 2013. A high-performance liquid chromatography/tandem mass spectrometry assay for the simultaneous measurement of acetylcholine and clozapine in microdialysis samples. Journal of Chromatography A.
Insulin-like growth factor-II and heparin are anti-apoptotic survival factors in human villous cytotrophoblast
Hills, F., Mehmet, H. and Sullivan, M. 2012. Insulin-like growth factor-II and heparin are anti-apoptotic survival factors in human villous cytotrophoblast. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 163 (1), pp. 11-16. https://doi.org/10.1016/j.ejogrb.2012.03.013
Superovulation, IGFBP-1 and birth weight.
Johnson, M., Irvine, R., Hills, F., Bolton, V., Abbas, A., Brooks, A., Allman, A., Chard, T. and Nicolaides, K. 1995. Superovulation, IGFBP-1 and birth weight. European Journal of Obstetrics, Gynaecology and Reproductive Biology. 59 (2), pp. 193-195.
Insulin-related growth factor binding protein-1 levels in ovum donation pregnancies.
Brooks, A., Johnson, M., Hills, F., Chard, T., Irvine, R. and Abdalla, H. 1995. Insulin-related growth factor binding protein-1 levels in ovum donation pregnancies. European Journal of Obstetrics, Gynaecology and Reproductive Biology. 59 (1), pp. 91-94.
Elevated levels of insulin-like growth factor binding protein-1 in fetal distress.
Crawford, R., Hills, F., Farkas, A. and Chard, T. 1995. Elevated levels of insulin-like growth factor binding protein-1 in fetal distress. British Journal of Obstetrics and Gynaecology. 102 (7), pp. 538-540.
Circulating levels of IGF-I and IGF-binding protein-1 throughout pregnancy: relation to birthweight and maternal weight.
Hills, F., English, J. and Chard, T. 1996. Circulating levels of IGF-I and IGF-binding protein-1 throughout pregnancy: relation to birthweight and maternal weight. Journal of Endocrinology. 148 (2), pp. 303-309. https://doi.org/10.1677/joe.0.1480303
Antenatal dexamethasone therapy does not affect circulating concentrations of insulin-like growth factor binding protein-1.
Ogueh, O., Hills, F., Chard, T. and Johnson, M. 1998. Antenatal dexamethasone therapy does not affect circulating concentrations of insulin-like growth factor binding protein-1. Human Reproduction. 13 (6), pp. 1714-1716. https://doi.org/10.1093/humrep/13.6.1714
Effects of co-trimoxazole, erythromycin, amoxycillin, tetracycline and chloroquine on sperm function in vitro
Hargreaves, C., Rogers, S., Hills, F., Rahman, F., Howell, R. and Homa, S. 1998. Effects of co-trimoxazole, erythromycin, amoxycillin, tetracycline and chloroquine on sperm function in vitro. Human Reproduction. 13 (7), pp. 1878-1886.
Heparin prevents programmed cell death in human trophoblast
Hills, F., Abrahams, V., Gonzalez-Timon, B., Francis, J., Cloke, B., Hinkson, L., Rai, R., Regan, L., Mor, G., Sullivan, M., Lam, E. and Brosens, J. 2006. Heparin prevents programmed cell death in human trophoblast. Molecular Human Reproduction. 12 (4), pp. 237-242.
A longitudinal study of maternal plasma insulin-like growth factor binding protein-1 concentrations during normal pregnancy and pregnancies complicated by pre-eclampsia
Anim-Nyame, N., Hills, F., Soorana, S., Steer, P. and Johnson, M. 2000. A longitudinal study of maternal plasma insulin-like growth factor binding protein-1 concentrations during normal pregnancy and pregnancies complicated by pre-eclampsia. Human Reproduction. 15 (10), pp. 2215-2219. https://doi.org/10.1093/humrep/15.10.2215
Interactions between progesterone receptor isoforms in myometrial cells in human labour
Pieber, D., Allport, V., Hills, F., Johnson, M. and Bennett, P. 2001. Interactions between progesterone receptor isoforms in myometrial cells in human labour. Molecular Human Reproduction. 7 (9), pp. 875-879. https://doi.org/10.1093/molehr/7.9.875
Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro
Mak, I., Brosens, J., Christian, M., Hills, F., Chamley, L., Regan, L. and White, J. 2002. Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro. Journal of Clinical Endocrinology and Metabolism. 87 (6), pp. 2581-2588. https://doi.org/10.1210/jc.87.6.2581
Progesterone represses interleukin-8 and cyclo-oxygenase-2 in human lower segment fibroblast cells and amnion epithelial cells
Loudon, J., Elliott, C., Hills, F. and Bennett, P. 2003. Progesterone represses interleukin-8 and cyclo-oxygenase-2 in human lower segment fibroblast cells and amnion epithelial cells. Biology of Reproduction. 69 (1), pp. 331-337.
The insulin-like growth factor system in mammalian pregnancy: a workshop report
Carter, A., Hills, F., O'Gorman, D., Robets, C., Soorana, S., Watson, C. and Westwood, M. 2004. The insulin-like growth factor system in mammalian pregnancy: a workshop report. Placenta. 25 (Supple), pp. S53-S56. https://doi.org/10.1016/j.placenta.2004.01.019
Imprinting of IGF2 P0 transcript and novel alternatively spliced INS-IGF2 isoforms show differences between mouse and human
Monk, D., Sanches, R., Arnaud, P., Apostolidou, S., Hills, F., Abu-Amero, S., Murrell, A., Friess, H., Reik, W. and Stanier, P. 2006. Imprinting of IGF2 P0 transcript and novel alternatively spliced INS-IGF2 isoforms show differences between mouse and human. Human Molecular Genetics. 15 (8), pp. 1259-1269. https://doi.org/10.1093/hmg/ddl041
Chronic fluoxetine differentially modulates the hippocampal microtubular and serotonergic system in grouped and isolation reared rats
Bianchi, M., Fone, K., Shah, A., Atkins, A., Dawson, L., Heidbreder, C., Hagan, J. and Marsden, C. 2009. Chronic fluoxetine differentially modulates the hippocampal microtubular and serotonergic system in grouped and isolation reared rats. European Neuropsychopharmacology. 19 (11), pp. 778-790. https://doi.org/10.1016/j.euroneuro.2009.06.005
Fluoxetine administration modulates the cytoskeletal microtubular system in the rat hippocampus
Bianchi, M., Shah, A., Fone, K., Atkins, A., Dawson, L., Heidbreder, C., Hows, M., Hagan, J. and Marsden, C. 2009. Fluoxetine administration modulates the cytoskeletal microtubular system in the rat hippocampus. Synapse. 63 (4), pp. 359-364. https://doi.org/10.1002/syn.20614
Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression
Monk, D., Arnaud, P., Frost, J., Hills, F., Stanier, P., Feil, R. and Moore, G. 2009. Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression. Human Molecular Genetics. 18 (16), pp. 3066-3074. https://doi.org/10.1093/hmg/ddp248
STOX1 is not imprinted and is not likely to be involved in preeclampsia.
Hills, F., Iglesias-Platas, I., Jebbink, J. and Monk, D. 2007. STOX1 is not imprinted and is not likely to be involved in preeclampsia. Nature Genetics. 39 (3), pp. 279-280. https://doi.org/10.1038/ng0307-279
Limited evolutionary conservation of imprinting in the human placenta
Hills, F., Apostolidou, S., Arnaud, P. and Monk, D. 2006. Limited evolutionary conservation of imprinting in the human placenta. Proceedings of the National Academy of Sciences. 103 (17), pp. 6623-6628. https://doi.org/10.1073/pnas.0511031103
Regulation of human villous trophoblast by insulin-like growth factors and insulin-like growth factor-binding protein-1
Hills, F., Chard, T., Elder, M. and Sullivan, M. 2004. Regulation of human villous trophoblast by insulin-like growth factors and insulin-like growth factor-binding protein-1. Journal of Endocrinology. 183 (3), pp. 487-496. https://doi.org/10.1677/joe.1.05867
The relationship between insulin and insulin-like growth factor binding protein-1 is modified by pre-eclampsia.
Anim-Nyame, N., Hills, F., Soorana, S., Steer, P. and Johnson, M. 2003. The relationship between insulin and insulin-like growth factor binding protein-1 is modified by pre-eclampsia. Gynecological Endocrinology. 17 (6), pp. 471-476. https://doi.org/10.1080/09513590312331290408
Polyclonal anti-tumor necrosis factor-alpha Fab used as an ancillary treatment for severe malaria
Looareesuwan, S., Sjorstrom, L., Krudsood, S., Wilairatana, P., Porter, R., Hills, F. and Warrell, D. 1999. Polyclonal anti-tumor necrosis factor-alpha Fab used as an ancillary treatment for severe malaria. The American Journal of Tropical Medicine and Hygiene. 61 (1), pp. 26-33. https://doi.org/10.4269/ajtmh.1999.61.26
Raised circulating levels of interleukin-6 in women with an intrauterine contraceptive device.
Wolley, J., Saleem, S., Hills, F., Salem, H., El-Nashar, E. and Chard, T. 1996. Raised circulating levels of interleukin-6 in women with an intrauterine contraceptive device. Gynecologic and Obstetric Investigation. 42 (4), pp. 241-243. https://doi.org/10.1159/000291972
Mechanism of action of the intrauterine contraceptive device: evidence for a specific biochemical deficiency in the endometrium
Seleem, S., Hills, F., Salem, H., El-Nashar, E. and Chard, T. 1996. Mechanism of action of the intrauterine contraceptive device: evidence for a specific biochemical deficiency in the endometrium. Human Reproduction. 11 (6), pp. 1220-1222.
Lack of evidence for a circadian rhythm of IGFBP-1 in the mother and fetus during labour.
Harding, S., Mensah, A., Hills, F., Howell, R. and Chard, T. 1995. Lack of evidence for a circadian rhythm of IGFBP-1 in the mother and fetus during labour. British Journal of Obstetrics and Gynaecology. 102 (11), pp. 891-893.
The effects of labor on maternal and fetal levels of insulin-like growth factor binding protein-1
Hills, F., Crawford, R., Harding, S., Farkas, F. and Chard, T. 1994. The effects of labor on maternal and fetal levels of insulin-like growth factor binding protein-1. American Journal of Obstetrics and Gynecology. 171 (5), pp. 1292-1295.