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ISSN 1470-0328/1471-0528 (Online) Volume 125 Issue 9 August 2018

An International Journal of
Obstetrics and Gynaecology

IN THIS ISSUE
• Editorial: BJOG launches the Research Methods Guides
• Research Methods Guide: A good study starts with a clearly defined
question
• Every Woman, Every Child’s ‘Progress in Partnership’ for stillbirths:
a commentary by the stillbirth advocacy working group
• Recurrence of vulval intraepithelial neoplasia following treatment
with cidofovir or imiquimod: results from a multicentre, randomised,
phase II trial (RT3VIN)
• Cassava flour slurry as a low-cost alternative to commercially
available gel for obstetrical ultrasound: a blinded non-inferiority
trial comparison of image quality

Reporting the best research in women’s health since 1902 www.bjog.org


INTERIM EDITOR-IN-CHIEF Michael Marsh, UK
BJOG An International Journal of
Obstetrics and Gynaecology

deput y editors-in-chief Patrick Chien, UK John Thorp, USA (BJOG Inspired Editor)
emer itus editor Philip J Steer, UK (BJOG on the Case Editor)
exe c u t ive s c i e n t i f i c e d i to r s Aris T Papageorghiou, UK Dimitrios Siassakos, UK
Sharon Cameron, UK
scientific editors Sherif Abdel-Fattah, UK Stratis Kolibianakis, Greece
Nynke van den Broek, UK Tak Yeung Leung, China
Rufus Cartwright, UK Pierre Martin-Hirsch, UK
Suneet P Chauhan, USA Raj Naik, UK
Justin Clark, UK Federico Prefumo, Italy
Elena Contro, Italy Makrina Savvidou, UK
William Dodson, USA Robert M Silver, USA
Stergios Doumouchtsis, UK Anne Steiner, USA
Donald Dudley, USA Austin Ugwumadu, UK
Linda Duska, USA Evelyn Verheijen, the Netherlands
Kacey Eichelberger, USA Jeffrey Wilkinson, USA
Tarek El-Toukhy, UK Steven S Witkin, USA
Bill Helm, UK
t r a ine e s c i e n t i f i c e d i to r s James MN Duffy, UK Alexander Friedman, USA
Jason Franasiak, USA Rui Wang, Australia
stat istical rev i ewers Sarah Hardoon, UK Lee Middleton, UK
Karla Hemming, UK (Research Methods Joan Morris, UK
Guides Editor) Jack Wilkinson, UK
Amy H Herring, USA Ly-mee Yu, UK
Steven Lane, UK
e d i to r i a l b oa rd Cande Ananth, USA Tze Kin Lau, China
Hesham Al-Inany, Egypt Raymond Li, China
Michael Belfort, USA Boon Lim, Australia (BJOG since 1902 Editor)
Vincenzo Berghella, USA Christine McCourt, UK
Gérard Bréart, France Errol Norwitz, USA
Jane Daniels, UK Anthony Odibo, USA
Elaine Denny, UK Friday Okonofua, Nigeria
Jan Deprest, Belgium Karl SJ Oláh, UK (BJOG Debate Editor)
Tao Duan, China Julian Robinson, USA
Caroline Hallissey, UK Michael Varner, USA
Julia Hussein, UK Kevan Wylie, UK
Eric Jauniaux, UK (BJOG since 1902 Editor) Jim Jun Zhang, China
Sean T Kehoe, UK
bjo g asso ciate s Katie Cornthwaite, UK (CPD Associate)
Natalie Cooper, UK (Research Methods Guides Editor)
Brett Einerson, USA (Journal Club Coordinator)
Jen Jardine, UK (Journal Club Coordinator)
Athol Kent, South Africa (Insights from outside BJOG)
Shona Kirtley, UK (Insights from outside BJOG)
Daniel Stott, UK (Podcast Lead)
manag ing editor Abigail Cantor, UK
content deve lopment editor Louisa Waite, UK
senior assistant editor Liz Watson, UK
editor ial assistant Dave Atha, UK
assistant editor Libby Brown, UK

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Volume 125, Number 9, August 2018

Contents
BJOG An International Journal of
Obstetrics and Gynaecology

BJOG Editor’s Choice


Research Methods Guide
1049 Wooden spoons and thromboprophylaxis in obstetrics
1057 A good study starts with a clearly defined question
J Thorp (USA)
S Lane (UK)
1051 Insights from outside BJOG
BJOG Inspired
A Kent, S Kirtley (South Africa, UK)
1064 Uterine anomalies − Latin anatomy reigns
Editorial K Olah (UK)

1056 Essential skills: BJOG launches the Research Methods Guides BJOG Debate
MS Marsh (UK)
The language of abortion: time to terminate TOP
Commentaries 1065 FOR: Mandating TOP reduces research visibility and
1058 Every Woman, Every Child’s ‘Progress in Partnership’ for stillbirths: engenders stigma
a commentary by the stillbirth advocacy working group Á Kavanagh, ARA Aiken (UK, USA)
E Ateva, H Blencowe, T Castillo, A Dev, M Farmer, M Kinney, 1066 AGAINST: ‘Termination of pregnancy’ is less likely than
SK Mishra, S Hopkins Leisher, S Maloney, V Ponce Hardy, ‘abortion’ to be misunderstood or cause distress
P Quigley, J Ruidiaz, D Siassakos, JE Stoner, C Storey, PJ Steer (UK)
ML Tejada de Rivero Sawers (USA, UK, South Africa, India,
Argentina, Mexico) BJOG since 1902
MC: Stillbirth: moving from advocacy to action DJ Dudley,
* RM Silver (USA)
1067 We should stop using incorrect Latin to describe parity and
use plain English instead
1062 Is this primip a nullip? The daily abuse of language in obstetrics PJ Steer (UK)
G Hughes (UK) 1096 When the balloon goes up
C Paul (UK)
Mini commentary
1163 Twin-to-twin-transfusion syndrome: from amniodrainage
1068 WHO recommendations, dollars and sense to laser
JN Robinson (USA) F Prefumo, E Jauniaux (Italy, UK)

Systematic reviews
1069 The safety of quinolones and fluoroquinolones in pregnancy: Review article
a meta-analysis
1109 Postpartum venous thromboembolism prophylaxis
E Yefet, N Schwartz, B Chazan, R Salim, S Romano, Z Nachum (Israel)
may cause more harm than benefit: a critical analysis of
1077 Antidepressant use during pregnancy and the risk of attention- international guidelines through an evidence-based lens
deficit/hyperactivity disorder in the children: a meta-analysis of A Kotaska (Canada)
cohort studies MC: Postpartum venous thromboembolism prophylaxis: harm
H-Y Jiang, C-T Peng, X Zhang, B Ruan (China)
* versus benefit R Arya (UK)
MC: Antidepressant use during pregnancy and ADHD risk in
* children: current knowledge T Boukhris (Canada) Epidemiology
1086 Safety of the balloon catheter for cervical ripening in outpatient care: 1118 The impact of isolated maternal hypothyroxinaemia on the
complications during the period from insertion to expulsion of a incidence of large-for-gestational-age infants: the Ma'anshan
balloon catheter in the process of labour induction: a systematic review Birth Cohort study
M Diederen, JSM Gommers, C Wilkinson, D Turnbull, BWJ Mol (the Y-d Zhu, Y Han, K Huang, B-b Zhu, S-q Yan, X Ge, S-s Zhou,
Netherlands, Australia) Y-y Xu, L-i Ren, J Sheng, W-j Pan, J-h Hao, P Zhu, F-b Tao
1097 Uterine caesarean closure techniques affect ultrasound findings and (China)
MC: Tidying up WC Dodson (USA)
maternal outcomes: a systematic review and meta-analysis *
SI Stegwee, IPM Jordans, LF van der Voet, PM van de Ven, JCF Ket,
CB Lambalk, CJM de Groot, WJK Hehenkamp, JAF Huirne
(the Netherlands)

* MC: Mini commentary


Contents

1127 Cardiorespiratory fitness, exercise haemodynamics and birth Imaging


outcomes: the Coronary Artery Risk Development in Young Adults
1179 Cassava flour slurry as a low-cost alternative to commercially
Study
available gel for obstetrical ultrasound: a blinded non-inferiority
AD Lane-Cordova, MR Carnethon, JM Catov, S Montag, CE Lewis,
trial comparison of image quality
PJ Schreiner, A Dude, B Sternfeld, SE Badon, P Greenland,
A Aziz, P Dar, F Hughes, C Solorzano, MM Muller, C Salmon,
EP Gunderson (USA)
M Salmon, N Benfield (USA, Democratic Republic of Congo, Canada)
MC: Pre-pregnancy cardiovascular indices and birth outcomes of
* subsequent pregnancies: a ‘sequential stress test’ revealing hidden * MC: Cost-effective innovations in low-resource settings
cardiovascular weakness? S Matsubara (Japan) OH Chang, JP Wilkinson (USA)
MC: Many of the causes of preterm birth and poor fetal growth are
* genetic and intergenerational and unlikely to be affected by short-
1186 Fetal brain imaging following laser surgery in twin-to-twin surgery
J Stirnemann, G Chalouhi, M Essaoui, N Bahi-Buisson, P Sonigo,
term interventions PJ Steer (UK) A-E Millischer, A Lapillonne, V Guigue, LJ Salomon, Y Ville (France)
1137 A prospective cause of death classification system for maternal
deaths in low and middle-income countries: results from the Global BJOG Exchange
Network Maternal Newborn Health Registry 1192 Re: Postpartum venous thromboembolism prophylaxis may
O Pasha, EM McClure, S Saleem, SS Tikmani, A Lokangaka, A Tshefu, cause more harm than benefit: a critical analysis of international
CL Bose, M Bauserman, M Mwenechanya, E Chomba, WA Carlo, guidelines through an evidence-based lens
AL Garces, L Figueroa, KM Hambidge, NF Krebs, S Goudar, AM Friedman (USA)
BS Kodkany, S Dhaded, RJ Derman, A Patel, PL Hibberd, F Esamai,
C Tenge, EA Liechty, JL Moore, DD Wallace, M Koso-Thomas, 1193 Author’s reply re: Postpartum venous thromboembolism
M Miodovnik, RL Goldenberg (Pakistan, USA, Democratic Republic prophylaxis may cause more harm than benefit: a critical analysis of
of the Congo, Zambia, Guatemala, India, Kenya) international guidelines through an evidence-based lens
MC: To reduce maternal mortality, we must know and respond to A Kotaska (Canada)
* women's personal stories M Mathai (UK)
1194 Re: Postpartum venous thromboembolism prophylaxis may
1145 The antepartum stillbirth syndrome: risk factors and pregnancy cause more harm than benefit: a critical analysis of international
conditions identified from the INTERGROWTH-21st Project guidelines through an evidence-based lens
JE Hirst, J Villar, CG Victora, AT Papageorghiou, D Finkton, PG Lindqvist (Sweden)
FC Barros, MG Gravett, F Giuliani, M Purwar, IO Frederick, R Pang,
1195 Author’s reply re: Postpartum venous thromboembolism
L Cheikh Ismail, A Lambert, W Stones, YA Jaffer, DG Altman,
prophylaxis may cause more harm than benefit: a critical analysis of
JA Noble, EO Ohuma, SH Kennedy, ZA Bhutta, for the Interna-
international guidelines through an evidence-based lens
tional Fetal and Newborn Growth Consortium for the 21st Century
A Kotaska (Canada)
(INTERGROWTH-21st) (UK, Brazil, USA, Italy, India, China, Kenya,
Oman, Pakistan, Canada) 1195 Re: Postpartum venous thromboembolism prophylaxis: harm versus
benefit
Fetal medicine A Kotaska (Canada)

1154 Preterm premature rupture of membranes is a collateral effect 1196 Author’s reply re: Postpartum venous thromboembolism
of improvement in perinatal outcomes following fetoscopic prophylaxis: harm versus benefit
coagulation of chorionic vessels for twin–twin transfusion R Arya (UK)
syndrome: a retrospective observational study of 1092 cases
1197 Re: Cassava flour slurry as a low-cost alternative to commercially
J Stirnemann, F Djaafri, A Kim, I Mediouni, L Bussieres, E Spaggiari,
available gel for obstetrical ultrasound: a blinded non-inferiority
C Veluppillai, A Lapillonne, E Kermorvant, J-F Magny, C Colmant,
trial comparison of image quality
Y Ville (France)
S Pandey, K Murdia (India)
1164 Efficacy of antenatal corticosteroids in preterm twins: the
1198 Author’s reply re: Cassava flour slurry as a low-cost alternative to
EPIPAGE-2 cohort study
commercially available gel for obstetrical ultrasound: a blinded non-
D Palas, V Ehlinger, C Alberge, P Truffert, G Kayem, F Goffinet,
inferiority trial comparison of image quality
P-Y Ancel, C Arnaud, C Vayssière (France)
N Benfield on behalf of the authors (USA)

Gynaecological oncology 1198 Re: The clinical utility of genetic testing of tissues from pregnancy
losses
1171 Recurrence of vulval intraepithelial neoplasia following treatment
Y-S Kim, CW Choi, J-Y Hwang, T-H Kim (Korea)
with cidofovir or imiquimod: results from a multicentre,
randomised, phase II trial (RT3VIN)
CN Hurt, SEF Jones, T-A Madden, A Fiander, AJ Nordin, R Naik,
N Powell, M Carucci, A Tristram (UK)
MC: Is cidofovir a better treatment than imiquimod for high-grade
* vulval intraepithelial neoplasia? C William Helm (UK)
BJOG An International Journal of
Obstetrics and Gynaecology

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1InternationalCommittee of Medical Journal Editors, JAMA 1993; 269; 2282–2286


2Committee on Publication Ethics guidelines www.publicationethics.org.uk/guidelines/code/

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