ABSTRACT
Preconception counseling plays a key role in preparing for a pregnancy. In couples
with a history of recurrent early pregnancy loss, counseling is of particular importance
because women are invariably more distressed and require reassurance that everything
possible is being done to avoid future pregnancy losses. Because their subsequent
pregnancies are more likely to be planned and these patients may be more willing to
adopt recommendations that have been offered to them, it becomes more important to
identify which investigations and interventions are the most beneficial. Several interventions
ranging from genetic testing to lifestyle changes and medications may have a positive
effect on the chances of a successful pregnancy. Early pregnancy monitoring and support
increases the chance of a live birth and helps to predict potential future pregnancy
complications. Recent research suggests that events that occur in the uterine decidua,
even before a woman knows she is pregnant, may have a significant impact on fetal
growth and the outcome of pregnancy. With this in mind, shifting future research and
clinical practice to focus on the periconceptual period and the very early stages
of pregnancy should offer significant benefits to the health of both the mother and
her infant. The overall aim should be to effectively use every pregnancy as the health-care
opportunity of two lifetimes.
KEYWORDS
Early pregnancy - preconception counseling - recurrent pregnancy loss
REFERENCES
- 1
Freda M C, Moos M K, Curtis M.
The history of preconception care: evolving guidelines and standards.
Matern Child Health J.
2006;
10
(5, Suppl)
S43-S52
- 2
Johnson K, Posner S F, Biermann J et al..
Recommendations to improve preconception health and health care—United States. A report
of the CDC/ATSDR Preconception Care Work Group; Select Panel on Preconception Care.
MMWR Recomm Rep.
2006;
55
(RR-60)
1-23
- 3
Boulet S L, Parker C, Atrash H.
Preconception care in international settings.
Matern Child Health J.
2006;
10
(5, Suppl)
S29-S35
- 4 American Academy of Pediatrics and American College of Obstetricians and Gynecologists
.Guidelines for Perinatal Care. 6th ed. Washington, DC: ACOG; 2007
- 5 Clinical Knowledge Summaries (CKS) .Pre-conception—advice and management. NHS. 2007. Available
at: http://www.cks.nhs.uk/pre_conception_advice_and_management Accessed May 2011
- 6
Posner S F, Johnson K, Parker C, Atrash H, Biermann J.
The national summit on preconception care: a summary of concepts and recommendations.
Matern Child Health J.
2006;
10
(5, Suppl)
S197-S205
- 7
Speidel J J, Harper C C, Shields W C.
The potential of long-acting reversible contraception to decrease unintended pregnancy.
Contraception.
2008;
78
(3)
197-200
- 8
Jauniaux E, Farquharson R G, Christiansen O B, Exalto N.
Evidence-based guidelines for the investigation and medical treatment of recurrent
miscarriage.
Hum Reprod.
2006;
21
(9)
2216-2222
- 9
Li T C, Makris M, Tomsu M, Tuckerman E, Laird S.
Recurrent miscarriage: aetiology, management and prognosis.
Hum Reprod Update.
2002;
8
(5)
463-481
- 10 Guideline G T. 17. The Investigation and Treatment of Couples with Recurrent First
Trimester and Second Trimester Miscarriage. London, UK: Royal College of Obstetricians
and Gynaecologists; 2011
- 11
American College of Obstetricians and Gynecologists .
ACOG practice bulletin. Management of recurrent pregnancy loss. Number 24, February
2001. (Replaces Technical Bulletin Number 212, September 1995).
Int J Gynaecol Obstet.
2002;
78
(2)
179-190
- 12 The Dutch Society of Obstetrics and Gynecology (NVOG) .Guideline Recurrent Miscarriage.
Utrecht, The Netherlands: The Dutch Society of Obstetrics and Gynaecology (NVOG);
2007
- 13
Franssen M T, Musters A M, van der Veen F et al..
Reproductive outcome after PGD in couples with recurrent miscarriage carrying a structural
chromosome abnormality: a systematic review.
Hum Reprod Update.
2011;
17
(4)
467-475
- 14
Musters A M, Repping S, Korevaar J C et al..
Pregnancy outcome after preimplantation genetic screening or natural conception in
couples with unexplained recurrent miscarriage: a systematic review of the best available
evidence.
Fertil Steril.
2011;
95
(6)
2153-2157
2157
e1-e3
- 15
Platteau P, Staessen C, Michiels A, Van Steirteghem A, Liebaers I, Devroey P.
Preimplantation genetic diagnosis for aneuploidy screening in patients with unexplained
recurrent miscarriages.
Fertil Steril.
2005;
83
(2)
393-397
quiz 525-526
- 16
Donoso P, Devroey P.
PGD for aneuploidy screening: an expensive hoax?.
Best Pract Res Clin Obstet Gynaecol.
2007;
21
(1)
157-168
- 17
Laurino M Y, Bennett R L, Saraiya D S et al..
Genetic evaluation and counseling of couples with recurrent miscarriage: recommendations
of the National Society of Genetic Counselors.
J Genet Couns.
2005;
14
(3)
165-181
- 18
Collins J, Diedrich K, Franks S ESHRE Capri Workshop Group et al.
Genetic aspects of female reproduction.
Hum Reprod Update.
2008;
14
(4)
293-307
- 19
Branch D W, Gibson M, Silver R M.
Clinical practice. Recurrent miscarriage.
N Engl J Med.
2010;
363
(18)
1740-1747
- 20
Carp H JA, Dirnfeld M, Dor J, Grudzinskas J G.
ART in recurrent miscarriage: preimplantation genetic diagnosis/screening or surrogacy?.
Hum Reprod.
2004;
19
(7)
1502-1505
- 21
Rai R, Regan L.
Recurrent miscarriage.
Lancet.
2006;
368
(9535)
601-611
- 22
Carp H, Toder V, Aviram A, Daniely M, Mashiach S, Barkai G.
Karyotype of the abortus in recurrent miscarriage.
Fertil Steril.
2001;
75
(4)
678-682
- 23
Ogasawara M, Aoki K, Okada S, Suzumori K.
Embryonic karyotype of abortuses in relation to the number of previous miscarriages.
Fertil Steril.
2000;
73
(2)
300-304
- 24
Rai R S, Regan L, Clifford K et al..
Antiphospholipid antibodies and beta 2-glycoprotein-I in 500 women with recurrent
miscarriage: results of a comprehensive screening approach.
Hum Reprod.
1995;
10
(8)
2001-2005
- 25
Rai R S, Clifford K, Cohen H, Regan L.
High prospective fetal loss rate in untreated pregnancies of women with recurrent
miscarriage and antiphospholipid antibodies.
Hum Reprod.
1995;
10
(12)
3301-3304
- 26
Grimbizis G F, Camus M, Tarlatzis B C, Bontis J N, Devroey P.
Clinical implications of uterine malformations and hysteroscopic treatment results.
Hum Reprod Update.
2001;
7
(2)
161-174
- 27
Saravelos S H, Cocksedge K A, Li T C.
Prevalence and diagnosis of congenital uterine anomalies in women with reproductive
failure: a critical appraisal.
Hum Reprod Update.
2008;
14
(5)
415-429
- 28
Homer H A, Li T C, Cooke I D.
The septate uterus: a review of management and reproductive outcome.
Fertil Steril.
2000;
73
(1)
1-14
- 29
Clifford K, Rai R, Regan L.
Future pregnancy outcome in unexplained recurrent first trimester miscarriage.
Hum Reprod.
1997;
12
(2)
387-389
- 30
Brigham S A, Conlon C, Farquharson R G.
A longitudinal study of pregnancy outcome following idiopathic recurrent miscarriage.
Hum Reprod.
1999;
14
(11)
2868-2871
- 31
Law K L, Stroud L R, LaGasse L L, Niaura R, Liu J, Lester B M.
Smoking during pregnancy and newborn neurobehavior.
Pediatrics.
2003;
111
(6 Pt 1)
1318-1323
- 32
Kendrick J S, Merritt R K.
Women and smoking: an update for the 1990s.
Am J Obstet Gynecol.
1996;
175
(3 Pt 1)
528-535
- 33
Troe E J, Raat H, Jaddoe V WV et al..
Smoking during pregnancy in ethnic populations: the Generation R study.
Nicotine Tob Res.
2008;
10
(8)
1373-1384
- 34
Mishra G D, Dobson A J, Schofield M J.
Cigarette smoking, menstrual symptoms and miscarriage among young women.
Aust N Z J Public Health.
2000;
24
(4)
413-420
- 35
Salihu H M, Sharma P P, Getahun D et al..
Prenatal tobacco use and risk of stillbirth: a case-control and bidirectional case-crossover
study.
Nicotine Tob Res.
2008;
10
(1)
159-166
- 36
Ekblad M, Gissler M, Lehtonen L, Korkeila J.
Prenatal smoking exposure and the risk of psychiatric morbidity into young adulthood.
Arch Gen Psychiatry.
2010;
67
(8)
841-849
- 37
Newnham J P, Patterson L, James I, Reid S E.
Effects of maternal cigarette smoking on ultrasonic measurements of fetal growth and
on Doppler flow velocity waveforms.
Early Hum Dev.
1990;
24
(1)
23-36
- 38
Falk L, Nordberg A, Seiger A, Kjaeldgaard A, Hellström-Lindahl E.
Smoking during early pregnancy affects the expression pattern of both nicotinic and
muscarinic acetylcholine receptors in human first trimester brainstem and cerebellum.
Neuroscience.
2005;
132
(2)
389-397
- 39
Werler M M.
Teratogen update: smoking and reproductive outcomes.
Teratology.
1997;
55
(6)
382-388
- 40
Lindbohm M L, Sallmén M, Taskinen H.
Effects of exposure to environmental tobacco smoke on reproductive health.
Scand J Work Environ Health.
2002;
28
(Suppl 2)
84-96
- 41
Roza S J, Verburg B O, Jaddoe V WV et al..
Effects of maternal smoking in pregnancy on prenatal brain development. The Generation
R Study.
Eur J Neurosci.
2007;
25
(3)
611-617
- 42
Kline J, Levin B, Kinney A, Stein Z, Susser M, Warburton D.
Cigarette smoking and spontaneous abortion of known karyotype. Precise data but uncertain
inferences.
Am J Epidemiol.
1995;
141
(5)
417-427
- 43
Armstrong B G, McDonald A D, Sloan M.
Cigarette, alcohol, and coffee consumption and spontaneous abortion.
Am J Public Health.
1992;
82
(1)
85-87
- 44
Windham G C, Swan S H, Fenster L.
Parental cigarette smoking and the risk of spontaneous abortion.
Am J Epidemiol.
1992;
135
(12)
1394-1403
- 45
Ness R B, Grisso J A, Hirschinger N et al..
Cocaine and tobacco use and the risk of spontaneous abortion.
N Engl J Med.
1999;
340
(5)
333-339
- 46
Chatenoud L, Parazzini F, di Cintio E et al..
Paternal and maternal smoking habits before conception and during the first trimester:
relation to spontaneous abortion.
Ann Epidemiol.
1998;
8
(8)
520-526
- 47
George L, Granath F, Johansson A LV, Olander B, Cnattingius S.
Risks of repeated miscarriage.
Paediatr Perinat Epidemiol.
2006;
20
(2)
119-126
- 48
Nielsen A, Hannibal C G, Lindekilde B E et al..
Maternal smoking predicts the risk of spontaneous abortion.
Acta Obstet Gynecol Scand.
2006;
85
(9)
1057-1065
- 49
Windham G C, Behren J, Waller K, Fenster L.
Exposure to environmental and mainstream tobacco smoke and risk of spontaneous abortion.
Am J Epidemiol.
1999;
149
(3)
243-247
- 50
Anderson K, Norman R J, Middleton P.
Preconception lifestyle advice for people with subfertility.
Cochrane Database Syst Rev.
2010;
(4)
CD008189
- 51
Rasch V.
Cigarette, alcohol, and caffeine consumption: risk factors for spontaneous abortion.
Acta Obstet Gynecol Scand.
2003;
82
(2)
182-188
- 52
Gardella J R, Hill III J A.
Environmental toxins associated with recurrent pregnancy loss.
Semin Reprod Med.
2000;
18
(4)
407-424
- 53
Kesmodel U, Wisborg K, Olsen S F, Henriksen T B, Secher N J.
Moderate alcohol intake in pregnancy and the risk of spontaneous abortion.
Alcohol Alcohol.
2002;
37
(1)
87-92
- 54
Florey C D.
EUROMAC. A European concerted action: maternal alcohol consumption and its relation
to the outcome of pregnancy and child development at 18 months. Methods.
Int J Epidemiol.
1992;
21
(Suppl 1)
S38-S39
- 55
Harlap S, Shiono P H.
Alcohol, smoking, and incidence of spontaneous abortions in the first and second trimester.
Lancet.
1980;
2
(8187)
173-176
- 56
Bakker R, Pluimgraaff L E, Steegers E AP et al..
Associations of light and moderate maternal alcohol consumption with fetal growth
characteristics in different periods of pregnancy: the Generation R Study.
Int J Epidemiol.
2010;
39
(3)
777-789
- 57
Jaddoe V WV, Bakker R, Hofman A et al..
Moderate alcohol consumption during pregnancy and the risk of low birth weight and
preterm birth. The Generation R study.
Ann Epidemiol.
2007;
17
(10)
834-840
- 58
Parazzini F, Chatenoud L, Di Cintio E et al..
Coffee consumption and risk of hospitalized miscarriage before 12 weeks of gestation.
Hum Reprod.
1998;
13
(8)
2286-2291
- 59
Domínguez-Rojas V, de Juanes-Pardo J R, Astasio-Arbiza P, Ortega-Molina P, Gordillo-Florencio E.
Spontaneous abortion in a hospital population: are tobacco and coffee intake risk
factors?.
Eur J Epidemiol.
1994;
10
(6)
665-668
- 60
Bech B H, Nohr E A, Vaeth M, Henriksen T B, Olsen J.
Coffee and fetal death: a cohort study with prospective data.
Am J Epidemiol.
2005;
162
(10)
983-990
- 61
Tolstrup J S, Kjaer S K, Munk C et al..
Does caffeine and alcohol intake before pregnancy predict the occurrence of spontaneous
abortion?.
Hum Reprod.
2003;
18
(12)
2704-2710
- 62
Matijasevich A, Barros F C, Santos I S, Yemini A.
Maternal caffeine consumption and fetal death: a case-control study in Uruguay.
Paediatr Perinat Epidemiol.
2006;
20
(2)
100-109
- 63
Infante-Rivard C, Fernández A, Gauthier R, David M, Rivard G E.
Fetal loss associated with caffeine intake before and during pregnancy.
JAMA.
1993;
270
(24)
2940-2943
- 64
Weng X, Odouli R, Li D K.
Maternal caffeine consumption during pregnancy and the risk of miscarriage: a prospective
cohort study.
Am J Obstet Gynecol.
2008;
198
(3)
e1-e8
- 65
de Maeyer J, Schepens P J, Jorens P G, Verstraete R.
Exposure to pentachlorophenol as a possible cause of miscarriages.
Br J Obstet Gynaecol.
1995;
102
(12)
1010-1011
- 66
Li D K, Odouli R, Wi S et al..
A population-based prospective cohort study of personal exposure to magnetic fields
during pregnancy and the risk of miscarriage.
Epidemiology.
2002;
13
(1)
9-20
- 67
Li D K, Janevic T, Odouli R, Liu L.
Hot tub use during pregnancy and the risk of miscarriage.
Am J Epidemiol.
2003;
158
(10)
931-937
- 68
Brandt L PA, Nielsen C V.
Job stress and adverse outcome of pregnancy: a causal link or recall bias?.
Am J Epidemiol.
1992;
135
(3)
302-311
- 69
Florack E IM, Zielhuis G A, Pellegrino J E, Rolland R.
Occupational physical activity and the occurrence of spontaneous abortion.
Int J Epidemiol.
1993;
22
(5)
878-884
- 70
McDonald A D, McDonald J C, Armstrong B et al..
Fetal death and work in pregnancy.
Br J Ind Med.
1988;
45
(3)
148-157
- 71
Aleman A, Althabe F, Belizán J, Bergel E.
Bed rest during pregnancy for preventing miscarriage.
Cochrane Database Syst Rev.
2005;
(2)
CD003576
- 72 World Health Organisation .United Kingdom: health profile. World Health Organisation
(WHO); 2008. Available at: http://www.who.int/gho/countries/gbr.pdf Accessed May 2011
- 73 World Health Organisation .United States: health profile. World Health Organisation
(WHO); 2008. Available at: http://www.who.int/gho/countries/usa.pdf Accessed May 2011
- 74
Metwally M, Ong K J, Ledger W L, Li T C.
Does high body mass index increase the risk of miscarriage after spontaneous and assisted
conception? A meta-analysis of the evidence.
Fertil Steril.
2008;
90
(3)
714-726
- 75
Sebire N J, Jolly M, Harris J P et al..
Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London.
Int J Obes Relat Metab Disord.
2001;
25
(8)
1175-1182
- 76
Metwally M, Tuckerman E M, Laird S M, Ledger W L, Li T C.
Impact of high body mass index on endometrial morphology and function in the peri-implantation
period in
women with recurrent miscarriage.
Reprod Biomed Online.
2007;
14
(3)
328-334
- 77
Cocksedge K A, Li T C, Saravelos S H, Metwally M.
A reappraisal of the role of polycystic ovary syndrome in recurrent miscarriage.
Reprod Biomed Online.
2008;
17
(1)
151-160
- 78
Veleva Z, Tiitinen A, Vilska S et al..
High and low BMI increase the risk of miscarriage after IVF/ICSI and FET.
Hum Reprod.
2008;
23
(4)
878-884
- 79
Lashen H, Fear K, Sturdee D W.
Obesity is associated with increased risk of first trimester and recurrent miscarriage:
matched case-control study.
Hum Reprod.
2004;
19
(7)
1644-1646
- 80
Fedorcsák P, Storeng R, Dale P O, Tanbo T, Abyholm T.
Obesity is a risk factor for early pregnancy loss after IVF or ICSI.
Acta Obstet Gynecol Scand.
2000;
79
(1)
43-48
- 81
Bellver J, Rossal L P, Bosch E et al..
Obesity and the risk of spontaneous abortion after oocyte donation.
Fertil Steril.
2003;
79
(5)
1136-1140
- 82
Metwally M, Saravelos S H, Ledger W L, Li T C.
Body mass index and risk of miscarriage in women with recurrent miscarriage.
Fertil Steril.
2010;
94
(1)
290-295
- 83
Helgstrand S, Andersen A MN.
Maternal underweight and the risk of spontaneous abortion.
Acta Obstet Gynecol Scand.
2005;
84
(12)
1197-1201
- 84
Maconochie N, Doyle P, Prior S, Simmons R.
Risk factors for first trimester miscarriage-results from a UK-population-based case-control
study.
BJOG.
2007;
114
(2)
170-186
- 85 Word Health Organisation .Report of a WHO technical consultation on birth spacing.
World Health Organisation (WHO); 2005. Available at: http://whqlibdoc.who.int/hq/2007/WHO_RHR_07.1_eng.pdf Accessed May 2011
- 86
Love E R, Bhattacharya S, Smith N C, Bhattacharya S.
Effect of interpregnancy interval on outcomes of pregnancy after miscarriage: retrospective
analysis of hospital episode statistics in Scotland.
BMJ.
2010;
341
c3967-
- 87
Christiansen O B, Andersen A M, Bosch E et al..
Evidence-based investigations and treatments of recurrent pregnancy loss.
Fertil Steril.
2005;
83
(4)
821-839
- 88
Rai R, Cohen H, Dave M, Regan L.
Randomised controlled trial of aspirin and aspirin plus heparin in pregnant women
with recurrent miscarriage associated with phospholipid antibodies (or antiphospholipid
antibodies).
BMJ.
1997;
314
(7076)
253-257
- 89
Backos M, Rai R, Baxter N, Chilcott I T, Cohen H, Regan L.
Pregnancy complications in women with recurrent miscarriage associated with antiphospholipid
antibodies treated with low dose aspirin and heparin.
Br J Obstet Gynaecol.
1999;
106
(2)
102-107
- 90
Empson M, Lassere M, Craig J C, Scott J R.
Recurrent pregnancy loss with antiphospholipid antibody: a systematic review of therapeutic
trials.
Obstet Gynecol.
2002;
99
(1)
135-144
- 91
Mak I YH, Brosens J J, Christian M et al..
Regulated expression of signal transducer and activator of transcription, Stat5, and
its enhancement of PRL expression in human endometrial stromal cells in vitro.
J Clin Endocrinol Metab.
2002;
87
(6)
2581-2588
- 92
Bose P, Black S, Kadyrov M et al..
Heparin and aspirin attenuate placental apoptosis in vitro: implications for early
pregnancy failure.
Am J Obstet Gynecol.
2005;
192
(1)
23-30
- 93
Di Simone N, Castellani R, Caliandro D, Caruso A.
Antiphospholid antibodies regulate the expression of trophoblast cell adhesion molecules.
Fertil Steril.
2002;
77
(4)
805-811
- 94
Sebire N J, Backos M, Gaddal S, Goldin R D, Regan L.
Placental pathology, antiphospholipid antibodies, and pregnancy outcome in recurrent
miscarriage patients.
Obstet Gynecol.
2003;
101
(2)
258-263
- 95
Bose P, Black S, Kadyrov M et al..
Adverse effects of lupus anticoagulant positive blood sera on placental viability
can be prevented by heparin in vitro.
Am J Obstet Gynecol.
2004;
191
(6)
2125-2131
- 96
Dolitzky M, Inbal A, Segal Y, Weiss A, Brenner B, Carp H.
A randomized study of thromboprophylaxis in women with unexplained consecutive recurrent
miscarriages.
Fertil Steril.
2006;
86
(2)
362-366
- 97
Badawy A M, Khiary M, Sherif L S, Hassan M, Ragab A, Abdelall I.
Low-molecular weight heparin in patients with recurrent early miscarriages of unknown
aetiology.
J Obstet Gynaecol.
2008;
28
(3)
280-284
- 98
Mantha S, Bauer K A, Zwicker J I.
Low molecular weight heparin to achieve live birth following unexplained pregnancy
loss: a systematic review.
J Thromb Haemost.
2010;
8
(2)
263-268
- 99
Kaandorp S, Nisio M, Goddijn M, Middeldorp S.
Aspirin or anticoagulants for treating recurrent miscarriage in women without antiphospholipid
syndrome.
Cochrane Database Syst Rev.
2009;
(1)
CD004734-
- 100
Kaandorp S P, Goddijn M, Post J A et al..
Aspirin plus heparin or aspirin alone in women with recurrent miscarriage.
N Engl J Med.
2010;
362
(17)
1586-1596
- 101
Li D K, Liu L Y, Odouli R.
Exposure to non-steroidal anti-inflammatory drugs during pregnancy and risk of miscarriage:
population based cohort study.
BMJ.
2003;
327
(7411)
368-371
- 102
Nielsen G L, Skriver M V, Pedersen L, Sørensen H T.
Danish group reanalyses miscarriage in NSAID users.
BMJ.
2004;
328
(7431)
109
- 103
George L, Mills J L, Johansson A LV et al..
Plasma foliate levels and risk of spontaneous abortion.
JAMA.
2002;
288
(15)
1867-1873
- 104
Timmermans S, Jaddoe V W, Hofman A, Theunissen R P, Steegers E A.
Periconception folic acid supplementation, fetal growth and the risks of low birth
weight and preterm birth: the Generation R study.
Br J Nutr.
2009;
102
(5)
777-785
- 105
Mook-Kanamori D O, Steegers E AP, Eilers P H, Raat H, Hofman A, Jaddoe V W.
Risk factors and outcomes associated with first-trimester fetal growth restriction.
JAMA.
2010;
303
(6)
527-534
- 106
George A, Shamim S, Johnson M et al..
Periodontal treatment during pregnancy and birth outcomes: a metaanalysis of randomised
trials.
Int J Evid-Based Healthcare.
2011;
9
(2)
122-147
- 107
Polyzos N P, Polyzos I P, Mauri D et al..
Effect of periodontal disease treatment during pregnancy on preterm birth incidence:
a metaanalysis of randomized trials.
Am J Obstet Gynecol.
2009;
200
(3)
225-232
- 108
Moore S, Ide M, Coward P Y et al..
A prospective study to investigate the relationship between periodontal disease and
adverse pregnancy outcome.
Br Dent J.
2004;
197
(5)
251-258
discussion 247
- 109
Farrell S, Ide M, Wilson R F.
The relationship between maternal periodontitis, adverse pregnancy outcome and miscarriage
in never smokers.
J Clin Periodontol.
2006;
33
(2)
115-120
- 110
Uppal A, Uppal S, Pinto A et al..
The effectiveness of periodontal disease treatment during pregnancy in reducing the
risk of experiencing preterm birth and low birth weight: a meta-analysis.
J Am Dent Assoc.
2010;
141
(12)
1423-1434
- 111
Khader Y S, Ta'ani Q.
Periodontal diseases and the risk of preterm birth and low birth weight: a meta-analysis.
J Periodontol.
2005;
76
(2)
161-165
- 112
Rumbold A, Middleton P, Pan N, Crowther C A.
Vitamin supplementation for preventing miscarriage.
Cochrane Database Syst Rev.
2011;
(1)
CD004073-
- 113
Shah P S, Ohlsson A. Knowledge Synthesis Group on Determinants of Low Birth Weight
and Preterm Births .
Effects of prenatal multimicronutrient supplementation on pregnancy outcomes: a meta-analysis.
CMAJ.
2009;
180
(12)
E99-E108
- 114
van Eijsden M, Hornstra G, van der Wal M F, Vrijkotte T G, Bonsel G J.
Maternal n-3, n-6, and trans fatty acid profile early in pregnancy and term birth
weight: a prospective cohort study.
Am J Clin Nutr.
2008;
87
(4)
887-895
- 115
Porter T F, LaCoursiere Y, Scott J R.
Immunotherapy for recurrent miscarriage.
Cochrane Database Syst Rev.
2006;
(2)
CD000112
- 116
Haas D M, Ramsey P S.
Progestogen for preventing miscarriage.
Cochrane Database Syst Rev.
2008;
(2)
CD003511
- 117
Scott J R, Pattison N.
Human chorionic gonadotrophin for recurrent miscarriage.
Cochrane Database Syst Rev.
2000;
(2)
CD000101
- 118
Stray-Pedersen B, Stray-Pedersen S.
Etiologic factors and subsequent reproductive performance in 195 couples with a prior
history of habitual abortion.
Am J Obstet Gynecol.
1984;
148
(2)
140-146
- 119
Liddell H S, Pattison N S, Zanderigo A.
Recurrent miscarriage-outcome after supportive care in early pregnancy.
Aust N Z J Obstet Gynaecol.
1991;
31
(4)
320-322
- 120
Jauniaux E, Jurkovic D, Henriet Y, Rodesch F, Hustin J.
Development of the secondary human yolk sac: correlation of sonographic and anatomical
features.
Hum Reprod.
1991;
6
(8)
1160-1166
- 121
Dickey R P, Gasser R F, Olar T T et al..
Risk of recurrent abortion after appearance of a chorionic sac or heart rate on vaginal
ultrasound.
Lancet.
1994;
344
(8934)
1442-1443
- 122
Dickey R P, Gasser R F, Olar T T et al..
The relationship of initial embryo crown—rump length to pregnancy outcome and abortus
karyotype based on new growth curves for the 2-31 mm embryo.
Hum Reprod.
1994;
9
(2)
366-373
- 123
Stampone C, Nicotra M, Muttinelli C, Cosmi E V.
Transvaginal sonography of the yolk sac in normal and abnormal pregnancy.
J Clin Ultrasound.
1996;
24
(1)
3-9
- 124
Makrydimas G, Sebire N J, Lolis D, Vlassis N, Nicolaides K H.
Fetal loss following ultrasound diagnosis of a live fetus at 6-10 weeks of gestation.
Ultrasound Obstet Gynecol.
2003;
22
(4)
368-372
- 125
Papaioannou G I, Syngelaki A, Maiz N, Ross J A, Nicolaides K H.
Ultrasonographic prediction of early miscarriage.
Hum Reprod.
2011;
26
(7)
1685-1692
- 126
Saraswat L, Bhattacharya S, Maheshwari A, Bhattacharya S.
Maternal and perinatal outcome in women with threatened miscarriage in the first trimester:
a systematic review.
BJOG.
2010;
117
(3)
245-257
- 127
Smith G C, Smith M F, Nay M B, Fleming J E.
First trimester growth and the risk of low birth weight.
N Engl J Med.
1998;
339
(25)
1817-1822
- 128
Bukowski R, Smith G C, Malone F D FASTER Research Consortium et al.
Fetal growth in early pregnancy and risk of delivering low birth weight infant: prospective
cohort study.
BMJ.
2007;
334
(7598)
836-
- 129
Pedersen N G, Figueras F, Tabor A, Gardosi J.
Early fetal size and growth as predictors of adverse outcome.
Obstet Gynecol.
2008;
112
(4)
765-771
- 130
Smith G CS.
First-trimester determination of complications of late pregnancy.
JAMA.
2010;
303
(6)
561-562
- 131
Law L W, Leung T Y, Sahota D S, Chan L W, Fung T Y, Lau T K.
Which ultrasound or biochemical markers are independent predictors of small-for-gestational
age?.
Ultrasound Obstet Gynecol.
2009;
34
(3)
283-287
- 132
Plasencia W, Maiz N, Poon L, Yu C, Nicolaides K H.
Uterine artery Doppler at 11þ0 to 13þ6 weeks and 21þ0 to 24þ6 weeks in the prediction
of pre-eclampsia.
Ultrasound
Obstet Gynecol.
2008;
32
(2)
138-146
- 133
Poon L CY, Stratieva V, Piras S, Piri S, Nicolaides K H.
Hypertensive disorders in pregnancy: combined screening by uterine artery Doppler,
blood pressure and serum PAPP-A at 11-13 weeks.
Prenat Diagn.
2010;
30
(3)
216-223
- 134
Plasencia W, Maiz N, Bonino S, Kaihura C, Nicolaides K H.
Uterine artery Doppler at 11þ0 to 13þ6 weeks in the prediction of pre-eclampsia.
Ultrasound Obstet Gynecol.
2007;
30
(5)
742-749
- 135
Leunissen R W, Kerkhof G F, Stijnen T, Hokken-Koelega A.
Timing and tempo of first-year rapid growth in relation to cardiovascular and metabolic
risk profile in early
adulthood.
JAMA.
2009;
301
(21)
2234-2242
- 136
Ekelund U, Ong K K, Linné Y et al..
Association of weight gain in infancy and early childhood with metabolic risk in young
adults.
J Clin Endocrinol Metab.
2007;
92
(1)
98-103
- 137
Ekelund U, Ong K, Linné Y et al..
Upward weight percentile crossing in infancy and early childhood independently predicts
fat mass in young adults: the Stockholm Weight Development Study (SWEDES).
Am J Clin Nutr.
2006;
83
(2)
324-330
- 138
Fagerberg B, Bondjers L, Nilsson P.
Low birth weight in combination with catch-up growth predicts the occurrence of the
metabolic syndrome in men at late middle age: the Atherosclerosis and Insulin Resistance
study.
J Intern Med.
2004;
256
(3)
254-259
- 139
Ramadhani M K, Grobbee D E, Bots M L et al..
Lower birth weight predicts metabolic syndrome in young adults: the Atherosclerosis
Risk in Young Adults (ARYA) study.
Atherosclerosis.
2006;
184
(1)
21-27
- 140
Vos L E, Oren A, Bots M L, Gorissen W H, Grobbee D E, Uiterwaal C S.
Birth size and coronary heart disease risk score in young adulthood. The Atherosclerosis
Risk in Young Adults (ARYA) study.
Eur J Epidemiol.
2006;
21
(1)
33-38
- 141
Geelhoed J JM, Verburg B O, Nauta J et al..
Tracking and determinants of kidney size from fetal life until the age of 2 years:
the Generation R study.
Am J Kidney Dis.
2009;
53
(2)
248-258
- 142
Poon L C, Akolekar R, Lachmann R, Beta J, Nicolaides K H.
Hypertensive disorders in pregnancy: screening by biophysical and biochemical markers
at 11-13 weeks.
Ultrasound Obstet Gynecol.
2010;
35
(6)
662-670
- 143
Goetzinger K R, Singla A, Gerkowicz S, Dicke J M, Gray D L, Odibo A O.
The efficiency of first-trimester serum analytes and maternal characteristics in predicting
fetal
growth disorders.
Am J Obstet Gynecol.
2009;
201
(4)
412; e1-e6
- 144
Goetzinger K R, Singla A, Gerkowicz S, Dicke J M, Gray D L, Odibo A O.
Predicting the risk of pre-eclampsia between 11 and 13 weeks' gestation by combining
maternal characteristics and serum analytes, PAPP-A and free b-hCG.
Prenat Diagn.
2010;
30
(12-13)
1138-1142
- 145
Cusick W, Rodis J F, Vintzileos A M, Albini S M, McMahon M, Campbell W A.
Predicting pregnancy outcome from the degree of maternal serum alpha-fetoprotein elevation.
J Reprod Med.
1996;
41
(5)
327-332
- 146
Williams M A, Hickok D E, Zingheim R W, Mittendorf R, Kimelman J, Mahony B S.
Low birth weight and preterm delivery in relation to early-gestation vaginal bleeding
and elevated maternal serum alpha-fetoprotein.
Obstet Gynecol.
1992;
80
(5)
745-749
- 147
Chandra S, Scott H, Dodds L, Watts C, Blight C, Van Den Hof M.
Unexplained elevated maternal serum alphafetoprotein and/or human chorionic gonadotropin
and the
risk of adverse outcomes.
Am J Obstet Gynecol.
2003;
189
(3)
775-781
- 148
Spencer K, Cowans N J, Chefetz I, Tal J, Meiri H.
First trimester maternal serum PP-13, PAPP-A and secondtrimester uterine artery Doppler
pulsatility index as markers of pre-eclampsia.
Ultrasound Obstet Gynecol.
2007;
29
(2)
128-134
- 149
Odibo A O, Zhong Y, Longtine M et al..
First-trimester serum analytes, biophysical tests and the association with pathological
morphometry in the placenta of pregnancies with preeclampsia and fetal growth restriction.
Placenta.
2011;
32
(4)
333-338
- 150
Pilalis A, Souka A P, Antsaklis P et al..
Screening for preeclampsia and fetal growth restriction by uterine artery Doppler
and PAPP-A at 11-14 weeks' gestation.
Ultrasound Obstet Gynecol.
2007;
29
(2)
135-140
- 151
Nicolaides K H, Bindra R, Turan O M et al..
A novel approach to first-trimester screening for early pre-eclampsia combining serum
PP-13 and Doppler ultrasound.
Ultrasound Obstet Gynecol.
2006;
27
(1)
13-17
- 152
Venkat-Raman N, Backos M, Teoh T G, Lo W TS, Regan L.
Uterine artery Doppler in predicting pregnancy outcome in women with antiphospholipid
syndrome.
Obstet Gynecol.
2001;
98
(2)
235-242
- 153
Smith G CS.
First trimester origins of fetal growth impairment.
Semin Perinatol.
2004;
28
(1)
41-50
- 154
Eckert J P, Fleming T P.
SAC review: The effect of nutrition and environment on the preimplantation embryo.
Obstetrician Gynaecol.
2011;
13
(1)
43-48
- 155
Kwong W Y, Wild A E, Roberts P, Willis A C, Fleming T P.
Maternal undernutrition during the preimplantation period of rat development causes
blastocyst abnormalities and programming of postnatal hypertension.
Development.
2000;
127
(19)
4195-4202
- 156
Bloomfield F H, Oliver M H, Hawkins P et al..
A periconceptional nutritional origin for noninfectious preterm birth.
Science.
2003;
300
(5619)
606
- 157
Watkins A J, Wilkins A, Cunningham C et al..
Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural
and cardiovascular abnormalities in offspring.
J Physiol.
2008;
586
(8)
2231-2244
- 158
Sinclair K D, Allegrucci C, Singh R et al..
DNA methylation, insulin resistance, and blood pressure in offspring determined by
maternal periconceptional B vitamin and methionine status.
Proc Natl Acad Sci U S A.
2007;
104
(49)
19351-19356
- 159
Watkins A J, Lucas E S, Torrens C et al..
Maternal low protein diet during mouse pre-implantation development induces vascular
dysfunction and altered renin-angiotensinsystem homeostasis in the offspring.
Br J Nutr.
2010;
103
(12)
1762-1770
- 160
Woods L L, Ingelfinger J R, Nyengaard J R, Rasch R.
Maternal protein restriction suppresses the newborn reninangiotensin system and programs
adult hypertension in rats.
Pediatr Res.
2001;
49
(4)
460-467
- 161
Teklenburg G, Salker M, Molokhia M et al..
Natural selection of human embryos: decidualizing endometrial stromal cells serve
as sensors of embryo quality upon implantation.
PLoS ONE.
2010;
5
(4)
e10258
- 162
Salker M, Teklenburg G, Molokhia M et al..
Natural selection of human embryos: impaired decidualization of endometrium disables
embryo-maternal interactions and
causes recurrent pregnancy loss.
PLoS ONE.
2010;
5
(4)
e10287-
- 163
Teklenburg G, Salker M, Heijnen C, Macklon N S, Brosens J J.
The molecular basis of recurrent pregnancy loss: impaired natural embryo selection.
Mol Hum Reprod.
2010;
16
(12)
886-895
- 164
Williams D.
Pregnancy: a stress test for life.
Curr Opin Obstet Gynecol.
2003;
15
(6)
465-471
Lesley ReganM.B.B.S. M.D. F.R.C.O.G.
Department of Obstetrics and Gynaecology, St. Mary's Campus, Imperial College London
Mint Wing, South Wharf Road, London W2 1PG, UK
eMail: l.regan@imperial.ac.uk