Seminars in Fetal & Neonatal Medicine (2005) 10, 325e332

www.elsevierhealth.com/journals/siny

Preconception care in diabetes

Gillian Hawthorne*

Newcastle Diabetes Centre, Newcastle General Hospital, Westgate Road,Newcastle upon Tyne, NE46BE, UK

KEYWORDSPreconception care;Diabetes

Summary Preconception care is key to improving the outcome of diabeticpregnancy. Despite evidence showing that preconception care reduces congenitalmalformation in the offspring of diabetic mothers, most women do not plan theirpregnancies with their diabetes team. Issues around managing this complexbehaviour include the quality of the relationship with health care providers and thewoman’s health care beliefs. The elements of good preconception care haverecently been defined, but there are problems around access to preconceptionservices. There is a small number of preconception services within England, Walesand Northern Ireland; provision of these services needs to be increased if the goalset by the NSF for diabetes is to be achieved.ª 2005 Elsevier Ltd. All rights reserved.

Preconception care in diabetes

Pregnancy outcome for women with diabetes hasgreatly improved during the 20th century. In thelate 1940s the perinatal mortality rate (PNMR) fordiabetic pregnancy in Copenhagen was 400/1000.1

A decade later this had declined to 185/100 and by1989e1992 the PNMR was 8/1000 for plannedpregnancies and 59/1000 for unplanned pregnancies.

Today diabetic women still have high-risk preg-nancies. Reports from Europe and the UK confirmthat there is a fivefold increased risk of stillbirthand a threefold increased risk of congenital anom-

* Tel.: C44 191 256 3393; fax: C44 191 256 3212.E-mail address: gillian.hawthorne@newcastle-pct.nhs.uk

1744-165X/$ - see front matter ª 2005 Elsevier Ltd. All rights resdoi:10.1016/j.siny.2005.04.006

aly in the offspring.2e8 We continue to be chal-lenged by the goal set at St Vincent’s in 1989 ofimproving pregnancy outcome to approximate thatof non-diabetic women.9

Effect of peri-conceptional glycaemiccontrol on pregnancy outcome

Babies of diabetic mothers are more at risk of havinga congenital malformation. Population studies showthis risk to be four times higher than that for babiesof non-diabetic mothers.2 Maternal diabetes isparticularly associated with an increased preva-lence of cardiac10 and neural tube defects, althoughall types of congenital malformations can occur.

erved.

326 G. Hawthorne

Congenital malformations occur early in preg-nancy. Organogenesis is completed by 10 weeks ofgestation, so any abnormal organ development willhave already taken place by this time. Interven-tions to prevent fetal abnormality must occur priorto this initial phase of cellular proliferation andorganization.

Effective preconception care was first demon-strated to reduce major congenital malformationsin offspring of diabetic mothers by Kurt Fuhrmann.11

He showed that by maintaining good glycaemiccontrol before and throughout pregnancy, thecongenital abnormality rate in the offspring ofthose pregnancies was 0.8%, compared with 7.5%in the offspring of women who did not receivepreconception care. This regimen predated theadvent of home blood glucose monitoring andincluded regular hospitalization. Although thisstrategy successfully reduced poor outcome ofpregnancy, it was considered inappropriate forroutine adoption in the UK.

The availability of widespread home blood glu-cose monitoring facilitated the development ofoutpatient preconception care. In the UK Steelshowed the advantage of establishing a preconcep-tion service as an integral part of diabetes carebeginning in adolescence.12 Women attending forpreconception diabetes care had lower HbA1cs inthe first trimester and fewer babies with congenitalmalformations. The findings of other reports of thesuccess of preconception care in reducing thecongenital malformation rate13e17 were confirmedby the Diabetes Control and Complications Trial in1993.18 This trial supportedpreconceptional intensivemanagement to reduce rates of congenital malfor-mation. One congenital malformation occurred inthe ‘intensive’ group (HbA1c 7.4C1.3%) comparedto eight malformations in the group on conventionaltherapy (HbA1c 8.1C1.7%) before pregnancy.

A meta-analysis of published studies of pre-conception care, focusing on the effect of glycae-mic control, was published in 2001. In 14 cohortstudies reviewed, major congenital malformationswere assessed among 1192 babies of mothers whohad received preconception care and 1459 babiesof mothers who had not. The pooled rate of majormalformations was lower in those who had re-ceived preconception care compared to those whohad not (2.1% compared with 6.5%).18

Preconception care is a key area of healthcare,19 and the evidence for its effectiveness indiabetes is compelling, so why has preconceptioncare not been widely adopted within diabetes andmaternity services? One stumbling block has beenthe confusion andduntil recentlydlack of consen-sus about what preconception care entails.

What is preconception care?

Preconception care aims to improve outcome ofpregnancy. Consensus about exactly what is in-volved in preconception care is still being de-veloped. However, the two main components are:

� imparting relevant information to improveknowledge;

� supporting women to modify their behaviourbased on the knowledge gained.

Requisite knowledge

Both the Scottish Intercollegiate Guidelines Net-work (SIGN) and Diabetes UKdand more recentlythe American Diabetes Associationdhave pub-lished recommendations describing the compo-nents and delivery of preconception. SIGNstrongly recommends that prepregnancy care isprovided by a multidisciplinary team, dieteticadvice should be available, and all women shouldbe prescribed folic acid.20 The essential compo-nents of care include review of the medical,obstetric and gynaecological history, advice onglycaemic control to optimize HbA1c, and screen-ing for diabetic complications. Before pregnancywomen should aim to have blood glucose between4 and 7 mmol/L preprandial. Diabetes UK’s adviceis similar but with additional emphasis on theinvolvement of the woman in decision-makingand the inclusion of the woman and her partneras members of the team.21 The ideal target forHbA1c is !6%; it is recognized that this may notalways be feasible, but HbA1c should at least beless than 7%. Targets for capillary whole bloodglucose before meals are !5.6 mmol/L and 2 hpost-meal !7.8 mmol/L. Women should be coun-selled about the risks of congenital malformations,possible obstetric complications, the potentialeffect of pregnancy on diabetic complicationsand pregnancy management according to localprotocols.

Relevant knowledge in a preconception pro-gramme as recommended by the American Di-abetes Association22 includes patient educationabout diabetes, pregnancy, family planning anddiabetes self-management skills. There should bephysician-directed medical care, and laboratorytesting and counselling by a mental health pro-fessional when indicated to reduce stress and sup-port the woman in her diabetes self-management.The goal is to obtain the lowest HbA1c possiblewithout hypoglycaemia.

Preconception care in diabetes 327

Supportive behaviour

So much for knowledgedmodification of behaviouris more difficult. In other areas of this type of care,health-care professionals consider preconceptioncare as best delivered opportunistically.23 This hasbeen shown to be acceptable to women of child-bearing age. However, recent experience in theformer Northern region of England of mothers whohad requested or had received preconceptionadvice is that congenital malformation rates werenot reduced.24 Our experience is that opportunis-tic preconception care in the context of routinediabetes clinics does not work. This experience issimilar to that of others, and there may be manyreasons for this.25 Self-management of diabetesinvolves complex behaviours and relies on thediabetic woman having an appropriate repertoireof knowledge, skills, beliefs, intentions and moti-vation.26 Diabetes education programmes havehad limited success because of over-reliance onpatient education.

Interestingly and counter-intuitively, womenwho have experienced prior complications withpregnancy are significantly more likely to enterpregnancy with suboptimal control of their bloodglucose levels than women who have not had a pre-vious pregnancy.27,28 Women who have not beengiven a target HbA1c to achieve have also beenshown to have a higher incidence of suboptimalglycaemic control.28 Casele et al.27 wondered ifpatient education by physicians was insufficient,but taking into account the results from the North-ern regiondwhere nurses were the primary educa-torsdit seems that the current format of educationdelivered by all health-care professionals is in-effective in terms of changing behaviour.

Do structured programmes of preconceptioncare fare any better? Evaluation of formal pro-grammes run in the US found that only 20e34% ofpregnant diabetic women had previously accessedpreconception care despite a variety of outreachefforts and widespread advertising.29,30 However,these North American studies may not be compa-rable to UK practice and populations.

Role of preconception clinics

Preconception clinics deliver preconception care.This is different from preconception counselling,which implies a one-time discussion. Care isa continuous process which is goal-oriented.

The provision of preconception care is recom-mended in the National Service Framework fordiabetes to achieve the standard for diabetes

and pregnancy which is good outcomes of pre-gnancy for women with preexisting diabetes.31 TheAmerican Diabetes Association recommends thatall women who have child-bearing potential shouldbe counselled about the risk of congenital malfor-mations associated with unplanned pregnancy andpoor metabolic control, and that women shoulduse effective contraception unless they are in goodmetabolic control and actively trying to con-ceive.23

So how do you do this in a preconception clinic?Care from the clinic has to be individualized tothe woman’s specific needs, and the womanshould be encouraged to attend with her partner.The multidisciplinary team needs to work inpartnership with the woman to support the goalof optimal glycaemic control as well as evaluatethe additional risks associated with diabetescomplications and previous obstetric history.There should be a clear management plan agreedwith appropriate targets for glycaemic controlset. Specific attention should be paid to the issuesdescribed below.

Hypoglycaemia

In some women with longstanding type 1 diabetes,attempts to achieve normal blood glucose levelscan precipitate frequent and sudden hypoglycae-mic episodes. Although hypoglycaemia does notdamage the fetus, it is unpleasant and representsa significant risk for the mother. Specific educationabout hypoglycaemia is required, including theissue of glucagon with instructions for use to thefamily and other supporters. Close contact withthe women is required to prevent hypoglycaemia.

Management of diabetic complications

Diabetic retinopathyDiabetic eye disease may worsen during pregnancy.Women need to be aware of their individual risk. Ifdiabetic eye disease is present, close surveillanceduring pregnancy and timely treatment arerequired.

HypertensionMany women will already be on treatment forhypertension. Although ACE inhibition is contra-indicated in pregnancy, ACE inhibitors are notteratogenic and can be continued until concep-tion.32 Usual practice involves switching thewomen’s antihypertensive medication to treat-ment such as methyldopa which is not contra-indicated in pregnancy.

328 G. Hawthorne

Diabetic nephropathyWomen known to have diabetic nephropathy priorto pregnancy need a baseline assessment of renalfunction; this will include 24 h urine for albuminexcretion and a creatinine clearance. Counsellingabout the specific risks to the pregnancy is re-quired. The outcome of pregnancy is generallygood in women with mild to moderate diabeticrenal insufficiency,33 although there is an in-creased risk of preeclampsia with the attendantrisks of intrauterine growth restriction and iatro-genic prematurity. No consensus exists on theeffect of pregnancy on progression of diabeticnephropathy to end-stage renal failure, althoughwomen with more severe disease are less likely torecover renal function after delivery.34,35 Hyper-tension should be managed aggressively.

Other complicationsA major contraindication to pregnancy is thepresence of ischaemic heart disease. There is anincreased maternal mortality in these pregnan-cies,36 although a small number of pregnancieshave been successful after coronary revasculari-zation. Women need to be counselled sensitivelybut honestly about the risks, and it is likely thatthey will need someone to provide ongoing psy-chological support during this time.

Another contraindication is diabetic gastropa-resis. Autonomic neuropathy can complicate andendanger pregnancy.

Factors influencing peri-conceptionalglycaemic control

There are well-recognized factors that impede thedelivery of successful preconception care. Theseinclude:

� pregnancy planning;� the individual’s characteristics and health

beliefs;� the quality of the relationship with health care

professionals.

Pregnancy planning

What is pregnancy planning? A planned pregnancyhas been defined as a pregnancy that was desiredbefore conception, when contraception was stop-ped for the purpose of becoming pregnant, and inwhich the woman attempted to achieve optimalblood glucose control before becoming pregnant.27

Diabetic women who plan their pregnancies areless likely to smoke, likely to have more education,attend for diabetes care 6 months before preg-nancy, be married, more satisfied with theirpartner relationship, and older. Women with a pre-vious unplanned pregnancy are unlikely to plana subsequent pregnancy regardless of the outcomeof the previous pregnancy.27 Positive relationshipswith health-care providers described as caring andsupportive are associated with planned pregnancy.Women who feel judged and/or disliked by theirhealth-care provider are more likely to have anunplanned pregnancy.27

The major barrier remains that at least 40-80%of women do not plan their pregnancies.25,27,28 Areview of 529 diabetic pregnancies delivered after20 weeks’ gestation within the former Northernregion between 1995 and 1999 found that in 45% ofbirths there were no recorded HbA1c results innotes from specialist diabetes services for the 13months before conception, and only 37% of di-abetic women were reviewed at clinic within 3months of conception. Those women in good ormoderate control had a risk of malformationstatistically similar to that of the backgroundpopulation. Women with poor control within 3months of conception had a fivefold increased riskof congenital malformation. Folic acid was re-corded as being taken preconception in 17% ofbirths and in the first trimester in 41% of births.Folic acid had not been taken or was not recordedas taken in 43% of births.24 These findings areconsistent with several previous studies in the USand UK,37,38 and demonstrates that preconceptioncare services are still not being accessed bya significant proportion of diabetic women.

Individual’s characteristics andhealth beliefs

Low functional health literacy measured by read-ing comprehension is associated with several fac-tors that may adversely impact birth outcomes.39

Women with low health literacy present later forprenatal care. They have higher markers for lowersocioeconomic status and are more likely to haveunplanned pregnancy.

Many women with diabetes have misconceptionsabout their fertility.40 A significant number ofwomen with unplanned pregnancies did not usecontraception because they believed that diabeteswould make it more difficult to conceive. Othermisconceptions include the harmful effects ofinsulin on the fetus and increased risks of oralcontraceptives.

Preconception care in diabetes 329

Most women with unplanned pregnancy feelunsupported.41 They feel that their partner doesnot understand the risks or how much effort ittakes for the woman to achieve good blood glucosecontrol.

A survey of attitudes to and knowledge ofmaternal diabetes relating to pregnancy in a di-abetes clinic setting42 has found that although 85%of women are aware that diabetes could affect thehealth of their baby, only 69% of the nulligravidaeand 83% of the multiparae were aware of the needfor preconception planning. Only 52% of nulligra-vidae and 28% of the multiparae reported theintention to seek advice before a future pregnancy.This survey concluded that although knowledgewas good it did not increase attendance for pre-conception care.

Quality of relationships with health-careprofessionals

Women with unplanned pregnancy are more likelyto be disadvantaged. They are poorer, more likelyto belong to a racial or ethnic minority, unmarriedand smokers. Knowledge of risk is not enough. Anincreasing knowledge and understanding about theassociated risks is not sufficient to achieve behav-iour change.

A woman who feels that her health-care pro-fessional is opposed to pregnancy may not developan agreed plan with the health-care professional.Actively discouraging pregnancy should be avoidedas it may result in a complete breakdown ofcommunication between the woman and health-care professional. The key seems to be a strongpositive relationship with the health-care provider.Many women with poor glycaemic control andunplanned pregnancies report feeling judged anddisliked by health professionals. In turn they arecharacterized by health professionals as neglect-ors and treated negatively. Women are less likelyto adhere to treatment if they feel that health-care professionals are controlling, directive, andnot responding to their personal needs and opin-ions.43 A positive supportive relationship withhealth-care professionals allows prepregnancy ad-vice to be included in the care agenda.44 It has alsobeen shown that women are more likely to take uppreconception care services if they have supportfrom their partners or female friends.45

Situational and emotional factors can be com-plex and deeply rooted. For example the attitudestoward contraception and social support for birthcontrol are highly correlated.46

Health promotion within the clinical settingincreases knowledge and understanding of risksbut is not always sufficient to achieve behaviourchange. Increased knowledge alone does not nec-essarily change behaviour as there may be a num-ber of other factors which also have a stronginfluence on behaviour. Achieving good glycaemiccontrol in the preconception period requires med-ical, practical and cognitive skills.40,41 Educationalone is not enough.

Improving cohesiveness of diabetesmaternity services

Consistent and robust structures to deliver pre-conception care are currently lacking in the UK.There is no integration between primary andspecialist care in delivery of this service. Indeedit is unclear where the responsibility for provisionof preconception care lies. The Northern regionstudy showed that there was no beneficial effecton pregnancy outcome of prepregnancy planningadvice given by diabetes staff in a diabetes clinicsetting (Table 1).There was little difference in theincidence of congenital malformation betweenthose who sought advice and those who did not,nor between those who were recorded as receivingadvice and those who were not.

This begs the question: who should be deliveringthis service and how do we make it effective? Isthis a role for primary care, and if not how do weconfigure effective specialized diabetes services?There is an increasing number of women who willbenefit from this service. Traditionally, thosewomen with type 1 diabetes have been targeted,but now there are increasing numbers of womenwith type 2 diabetes who are of child-bearing age.How do we develop a preconception service acces-sible to them?

Table 1 Number and percentage of births for whichthe mother had requested advice or had receivedadvice on planning pregnancy prepregnancy and theeffect on congenital malformation rate, 1995e1999

Advice Number (%) Congenital malformation

Rate Odds ratio (95% CI)

Requested:Yes 230 (43.5) 78.3 4.0 (2.5, 6.6)No 299 (56.5) 83.6 4.3 (2.9, 6.6)

Received:Yes 284 (53.7) 81.0 4.2 (2.7, 6.4)No 245 (46.3) 81.6 4.2 (2.7, 6.7)

330 G. Hawthorne

Access to preconception care

The NHS has committed to the provision of pre-conception care in the National Service framework(NSF) for diabetes: Standard 9.47 This standardsays that diabetes service planning should includethe provision of preconception care and the pro-vision of advice to all women of child-bearing agewith diabetes about the importance of good bloodglucose control before and during pregnancy.

The preconception clinic service model sug-gested by the NSF for diabetesdservice modelsdisa clinic run jointly by the adult diabetes serviceand the maternity service for women wishing tobecome pregnant.48 The services provided by thisclinic should include optimization of glycaemiccontrol, advice on benefits of stopping smoking,dietary advice, advice on physical activity, folicacid supplementation, assessment of diabetescomplications and review of medications.

Despite this recommendation the CEMACH sur-vey in 2002 of the provision of preconceptionclinics as part of maternity services to diabeticwomen in England, Wales and Northern Irelandfound that only 17% of all units provided dedicatedtime and expertise within a separate preconcep-tion clinic.49 Of diabetes services, 49% providedpreconception counselling within the general di-abetes clinic, and 16% had no formal arrangementsat all (Table 2). This obviously falls considerablyshort of the NSF’s recommendation. There hasbeen little improvement in preconception caresince 1992,50 possibly reflecting that this is nota priority for many areas despite frequent effortsto highlight this deficiency.51

Strategies to improve the delivery of precon-ception care to women must become a priority for

Table 2 Provision of preconception counselling

Arrangements for preconceptioncounselling

Units

na %

Advice within the general diabetesclinic only

103 49

No formal arrangements for counselling 36 17Separate preconception clinic 35 17Other arrangements 17 8Advice within the general diabetesclinic and by an obstetrician within

the obstetric services

13 6

Advice by an obstetrician within theobstetric services only

7 3

a nZ211; two of the 213 units who returned a question-naire did not respond to the question on preconceptioncounselling.

the newly created managed diabetes networks.Their role is to deliver the standards of the NSF indiabetes by 2013, and clearly the delivery ofpreconception care is within their mandate. Canwe hope that all areas in England will havea network of specialized preconception clinicssupporting all diabetic women of child-bearingage within the next decade?

Practice points: preconception clinic

� Multidisciplinary team including diabetesnurse, dietician, physician and obstetrician.

� Set target levels for glycaemic control.� Folic acid to start 3 months before contra-

ception stopped.� Support to stop smoking.� Management of contraception.� Review of diabetic complications and

advice about risks during pregnancy.� Obstetric history review.� Discussion about expectations of pregnancy.� Referral for infertility treatment if appro-

priate.

Clinical practice points

� Preconception care reduces major congen-ital malformations in offspring of diabeticmothers.

� All women who have child-bearing poten-tial should be counselled about the risk ofmalformations associated with unplannedpregnancy and poor metabolic control.

� Prepregnancy care should be provided bya multidisciplinary team, dietetic adviceshould be available, and folic acid shouldbe prescribed.

� 40e80% of women with diabetes do notplan their pregnancies.

� A strong positive relationship with thehealth-care provider facilitates pregnancyplanning.

� NSF for diabetes advises that there shouldbe provision of preconception care to allwomen of child-bearing age with diabetes.

� 17% of units in England, Wales and North-ern Ireland provide a separate preconcep-tion clinic.

Preconception care in diabetes 331

References

1. Molsted-Pedersen L. The Pedersen legacy. In: Hod M,Jovanovic L, di Renzo GC, de Leiva A, Langer O, editors.Diabetes and pregnancy. Martin Dunitz; 2003. p. 23e9.

2. Hawthorne G, Robson S, Ryall EA, Sen D, Roberts SH, WardPlatt MP. Prospective population based survey of outcomeof pregnancy in diabetic women: results of the NorthernDiabetic Pregnancy Audit 1994. Br Med J 1997;315:279e81.

3. Casson I, Clark CA, Howard CV, McKendrick O, Pennycook S,Pharaoh PD, et al. Outcomes of pregnancy in insulindependent diabetic women: results of a five year popula-tion cohort study. Br Med J 1997;315:275e8.

4. Lauenborg J, Matheson E, Ovesen P, Westergaard JG,Ekbom P, Molsted-Pedersen L, et al. Audit on stillbirths inwomen with pregestational Type 1 diabetes. Diabetes Care2003;26:1385e9.

5. Hadden DR, Alexander A, McCance DR, Traub AI. Obstetricand diabetic care for pregnancy in diabetic women: 10years outcome analysis 1985e1995. Diabet Med 2001;18:546e53.

6. Diabetes and Pregnancy Group, France. French multicentricsurvey of outcome of pregnancy in women. Diabetes Care2003;26:2990e3.

7. Von Kries R, Kimmerle R, Schmidt JE, Hachmeister A,Bohm O, Wolf HG. Pregnancy outcomes in mothers with pre-gestational diabetes: a population-based study in NorthRhine [Germany] from 1988 to 1993. Eur J Pediatr 1997;156:963e7.

8. Evers IM, de Valk HW, Visser GHA. Risk of complications ofpregnancy in women with type 1 diabetes: nationwideprospective study in the Netherlands. Br Med J 2004;328:915e8.

9. Workshop Report. Diabetes care and research in Europe:the St Vincent declaration. Diabet Med 1990;7:360.

10. Wren C, Birrell G, Hawthorne G. Cardiovascular malforma-tions in infants of diabetic mothers.Heart 2003;89:1217e20.

11. Fuhrman K, Reiher H, Semmler K, Fischer F, Fischer M,Glockner E. Prevention of congenital malformations ininfants of insulin-dependent diabetic mothers. DiabetesCare 1983;6:219e23.

12. Steel JM, Johnstone FD, Hepburn D, Smith AF. Can pre-pregnancy care of diabetic women reduce the risk ofabnormal babies? Br Med J 1990;301:1070e3.

13. Damm P, Molsted-Pederson L. Significant decrease incongenital malformations in newborn infants of an un-selected population of diabetic women. Am J ObstetGynecol 1989;161:1163e7.

14. Goldman JA, Dicker D, Feldberg D, Yeshaya A, Samuel N,Karp M. Pregnancy outcome in patients with insulin-dependent

Research agenda: planning pregnancy

� Explore how women with type 1 diabetesunderstand their condition and the impli-cations of pregnancy.

� Identify social contexts that influence howdiabetic women manage pregnancy risk.

� Explore cultural contexts of pregnancyplanning for ethnic minority groups.

diabetes mellitus with preconceptional diabetic control:a comparative study. Am J Obstet Gynecol 1986;293e7.

15. Kitzmiller JL, Buchanan TA, Kjos S, Combs CA, Ratner RE. Pre-conception care of diabetes, congenital malformations andspontaneous abortions. Diabetes Care 1996;19:514e41.

16. Mills JL, Knopp RH, Simpson JL, Jovanovic-Peterson L,Metzger BE, Holmes LB, et al. Lack of relation of increasedmalformation rates in infants of diabetic mothers toglycemic control during organogenesis. N Engl J Med 1988;318:67e676.

17. The Diabetes Control and Complication Trial. Pregnancyoutcomes in the Diabetes Control and Complications Trial.Am J Obstet Gynecol 1996;174:1343e53.

18. Ray JG, O’Brien TE, Chan WS. Preconception care and therisk of congenital anomalies in the offspring of womenwith diabetes mellitus: a meta-analysis. Q J Med 2001;94:435e44.

19. House of Commons Health Committee. Maternity services:preconception. Health committee 4th report. London:HMSO; 1991.

20. Scottish Intercollegiate Guidelines Network 55. Manage-ment of diabetes in pregnancy 2002. !http://www.sign.ac.uk/guidelines/fulltext/55/section8.htmlO.

21. Preconception care for women with diabetes. Diabetes UK.!http://www.diabetes.org.ukO.

22. American Diabetes Association. Preconception care of womenwith diabetes. Diabetes Care 2003;26(Suppl. 1):S91e3.

23. Wallace M, Hurwitz B. Preconception care: who needs it,who wants it and how should it be provided? British Journalof General Practice 1998;48:963e6.

24. Bailey K. An analysis of data from an 8-year prospectivepopulation based survey of outcome of pregnancy indiabetic women in the north of England. Master of PublicHealth dissertation; 2003.

25. Rodgers BD, Rodgers DE. Efficacy of preconception care ofdiabetic women in a community setting. J Reprod Med1996;41:422e5.

26. Glasgow RE, McCaul KD, Schafer LC. Self-care behavioursand glycemic control in type 1 diabetes. J Chron Dis 1987;40:399e412.

27. Holing E, Beyer CS, Brown Z, Connell FA. Why don’t womenwith diabetes plan their pregnancies? Diabetes Care 1998;21:889e95.

28. Casele HL, Laifer SA. Factors influencing preconceptioncontrol of glycemia in diabetic women. Arch Intern Med1998;158:1321e4.

29. Cousins L, Kitzmiller J, Schneider J, Pierce J, McCoig D,DeVore S, et al. The California diabetes and pregnancyprogram: implementation of a multicenter experience withdiabetic pregnancies. J Perinatol 1992;12:173e80.

30. Wilhoite MB, Bennert Jr HW, Palomaki GE, Zaremba MM,Herman WH, Williams JR, et al. The impact of preconcep-tion counselling on pregnancy outcomes. Diabetes Care1993;16:450e5.

31. Department of Health. National Service Framework fordiabetes: standards. Department of Health; 2002.

32. Lip GYH, Churchill D, Beevers M, Auckett A, Beevers DG.Angiotensin converting enzyme inhibitors in earlypregnancy. Lancet 1997;350:1446e7.

33. Dunne FP, Chowdhury TA, Hartland A, Smith T, Brydon PA,McConkey C, et al. Pregnancy outcome in women withinsulin-dependent diabetes mellitus complicated by ne-phropathy. Q J Med 1999;92:451e4.

34. Biesenbach G, Grafinger P, Stoger H, Zazgornik J. Howpregnancy influences renal function in nephropathic type 1diabetic women depends on their pre-conceptual creatinineclearance. J Nephrol 1999;12:41e6.

332 G. Hawthorne

35. Rossing K, Jacobsen P, Hommel E, Mathieson E,Svenningsen A, Rossing P, et al. Pregnancy and progressionof diabetic nephropathy. Diabetologia 2002;45:36e41.

36. Bagg W, Henley PG. Pregnancy in women with diabetes andischaemic heart disease. Aust NZ Obstet Gynaecol 1999;39:99e102.

37. Rosenberg KD, Gelow J, Sandoval AP. Pregnancy intended-ness and the use of periconceptional folic acid. Pediatrics2003;111:1142e6.

38. Hellerstedt WL, Pirie PL, Lando HA, Curry SJ. Differences inpreconceptual and prenatal behaviours in women withintended and unintended pregnancies. Am J Public Health1998;88:663e7.

39. Endres LK, Sharp LK, Haney E, Dooley SL. Health literacyand pregnancy preparedness in pregestational diabetes.Diabetes Care 2004;27:331e5.

40. Rao S, Lindow SW, Masson EA. Survey of preconceptioncounselling. Diabet Med 2002;19:615.

41. Bloomgarden ZT, Karmally W, Metzger MJ, Brothers M,Nechmas C, Bookman J, et al. Randomised controlled trialof diabetic patient education: improved knowledgewithout improved metabolic status. Diabetes Care 1987;10:263e72.

42. Glasgow RE. Social-environmental factors in diabetes:barriers to diabetes self-care. In: Bradley C, editor.

Handbook of psychology and diabetes. London: HarwoodAcademic Publishers; 1994. p. 335e49.

43. Street Jr RL, Piziak VK, Carpentier WS, Herzog J, Hejl J,Skinner G, et al. Provider-patient communication andmetabolic control. Diabetes Care 1993;16:714e21.

44. Coustan D. Preconception planning. The relationship is thething. Diabetes Care 1998;21:8887e8.

45. Murphy DJ, Williamson PS, Nease DE. Supportive familymembers of diabetic adults. Fam Pract 1994;14:323e31.

46. St James PJ, Younger MD, Hamilton BD, Waisbren SE.Unplanned pregnancies in young women with diabetes.Diabetes Care 1993;16:1572e8.

47. Department of Health. National Service Framework fordiabetes: standards. Department of Health; 2001. p. 35[Diabetes and pregnancy].

48. Service models for consultation. NSF Diabetes: Servicemodels. p. 39. !http://www.dh.gov.uk.O

49. Confidential enquiry into maternal and child health.Maternity services in 2002 for women with type 1 and type2 diabetes. RCOG Press; 2004.

50. Brown CJ, Dawson A, Dodds R, Gamsu H, Gillmer M, Hall M,et al. Report of Pregnancy and Neonatal Care Group. DiabetMed 1996;13:S43e53.

51. Hawthorne G, Modder J. Maternity services for women withdiabetes in the UK. Diabet Med 2002;19(Suppl. 4):50e5.