Content uploaded by Karoline Kragelund Nielsen
Author content
All content in this area was uploaded by Karoline Kragelund Nielsen on Oct 17, 2018
Content may be subject to copyright.
Review Article
Prevention of Type 2 diabetes after gestational diabetes
directed at the family context: a narrative review from
the Danish Diabetes Academy symposium
K. Kragelund Nielsen
1,2,3
, L. Groth Grunnet
2,3,4
and H. Terkildsen Maindal
1,5
on behalf of
the Danish Diabetes Academy Workshop and Workshop Speakers
1
Health Promotion Research, Steno Diabetes Center Copenhagen, Gentofte,
2
Department of Public Health, University of Copenhagen, Copenhagen,
3
The Danish
Diabetes Academy, Odense,
4
Department of Endocrinology, Rigshospitalet, Copenhagen and
5
Department of Public Health, Aarhus University, Aarhus, Denmark
Accepted 9 March 2018
Abstract
In this review, we aim to summarize knowledge about gestational diabetes mellitus (GDM) after delivery; with special
focus on the potential of preventing Type 2 diabetes in a family context. The review expands on the key messages from a
symposium held in Copenhagen in May 2017 and highlights avenues for future research. A narrative review of the
symposium presentations and related literature is given. GDM is associated with increased short- and long-term adverse
outcomes including Type 2 diabetes for both mother and offspring. Interestingly, GDM in mothers also predicts diabetes
in the fathers. Thus, although GDM is diagnosed in pregnant women, the implications seem to affect the whole family.
Structured lifestyle intervention can prevent or delay the onset of Type 2 diabetes. In this review, we show how
numerous challenges are present in the target group, when such interventions are sought and implemented in real-world
settings. Although interlinked and interacting, barriers to maintaining a healthy lifestyle post-partum can be grouped
into those pertaining to diabetes beliefs, the family context and the healthcare system. Health literacy level and
perceptions of health and disease risk may modify these barriers. There is a need to identify effective approaches to
health promotion and health service delivery for women with prior GDM and their families. Future efforts may benefit
from involving the target group in the development and execution of such initiatives as one way of ensuring that
approaches are tailored to the needs of individual women and their families.
Diabet. Med. 35, 714–720 (2018)
Introduction
Gestational diabetes mellitus (GDM) has implications for the
health of both mother and offspring across the life course.
GDM has recently been defined by the American Diabetes
Association as ‘diabetes diagnosed in the second or third
trimester of pregnancy that was not clearly overt diabetes
prior to gestation’ [1]. Globally, GDM affects approximately
one in seven births, making it one of the most common
complications in pregnancy [2]. Although over past decades
there has been mounting evidence of the challenges and
benefits of detecting, diagnosing and treating GDM during
pregnancy in the short term, much remains to be understood
about the long-term adverse consequences of GDM, espe-
cially how these may be averted in real-life settings.
The family context may be an important yet overlooked
setting for diabetes prevention. It is well known that the
family context is an important condition for health and
disease. Part of this is due to biology; family members may
share genetics and hereditary predispositions. The intrauter-
ine environment also impacts long-term health outcomes
such as obesity, cardiovascular disease and diabetes [3]; where-
fore, parental exposure may affect offspring through fetal
programming and epigenetic effects that may even span
generations [4]. Members of the same family also often share
the same environment; they are exposed to many of the same
social and physical factors, e.g. pollutants, and behaviours
tend to be patterned according to social and economic
factors, and regularly cluster. Thus, studies suggest that, for
example, physical activity and eating patterns cluster among
family members in the same household [5,6]. Understanding
the social context in which a family exists and in which peo-
ple live their everyday lives is important for understanding
Correspondence to: Karoline Kragelund Nielsen.
E-mail: Karoline.Kragelund.Nielsen@regionh.dk
714 ª2018 Diabetes UK
DIABETICMedicine
DOI: 10.1111/dme.13622
why some people remain healthy while others develop
diseases.
The potential for Type 2 diabetes prevention after a GDM-
affected pregnancy in a family context was discussed at a
symposium arranged by the Danish Diabetes Academy in
Copenhagen, Denmark in May 2017. The aim of the
symposium was to explore and discuss current evidence on
and the potential for the prevention of Type 2 diabetes in
families affected by GDM. Existing evidence, challenges and
opportunities were presented by several speakers from
Denmark, Australia, Canada and Ireland, who were invited
based on their expertise in the area as well as their
experiences with intervention development and evaluation.
Here, we summarize existing knowledge about GDM in a
family context with a special focus on the potential for
prevention of Type 2 diabetes; expanding upon the presen-
tations and discussions from the symposium and highlighting
avenues for future research and practice.
How does GDM affect the short- and
long-term health of the mother, offspring
and father?
The importance of circumstances and risk factors throughout
the life course for adult disease has gained increasing
recognition in the past decade, including exposures encoun-
tered in early life and during pregnancy. GDM has been
shown to be associated with various short- and long-term
adverse health outcomes for not only the woman with GDM,
but also her offspring and even her partner.
Mother
Women who develop GDM have an increased risk of pre-
eclampsia, gestational hypertension and caesarean section
during pregnancy and delivery compared with their normo-
glycaemic counterparts [7,8]. Importantly, women with
GDM have a high rate (30–84%) of GDM reoccurrence in
subsequent pregnancies [9]. In the longer term, a history of
GDM is associated with an increased risk of Type 2 diabetes
[10]. An estimated 30–70% of women with GDM develop
diabetes within 15 years after the index GDM pregnancy
[10]. A meta-analysis including 20 studies showed that
women who have had GDM have at least a seven-fold
increased risk of developing Type 2 diabetes in the future
compared with women with a normoglycaemic pregnancy
[11]. Reported conversion rates from GDM to Type 2
diabetes vary by the length of follow-up, cohort retention
and ethnicity. Furthermore, studies also suggest that women
with a history of GDM are at higher risk of developing
cardiovascular disease and at a younger age compared with
women without GDM [12]. A recent large cohort study
demonstrated that GDM in mothers was associated with
independent post-partum diabetes, hypertension and cardio-
vascular disease, and that the magnitude of the association
increases sharply in combination with gestational hyperten-
sion [13].
Offspring
In the perinatal period, GDM is associated with an increased
risk of preterm delivery, macrosomia and adiposity in the
offspring [7,8]. However, studies suggest that the intrauter-
ine hyperglycaemic environment in mothers with GDM may
also place the offspring at an increased long-term risk for
metabolic disorders. According to the developmental origin
of health and disease hypothesis, a foetus can be pro-
grammed in utero to develop Type 2 diabetes and metabolic
disease later in life [14]. Thus, transient insults or adverse
intrauterine conditions such as undernutrition or overnutri-
tion –the latter by, for example, hyperglycaemia occurring
at critical points during development –may induce perma-
nent adaptive programming in key organs potentially medi-
ated by epigenetic mechanisms. The ‘Pedersen hypothesis’
suggested 50 years ago that fetal overgrowth is related to
increased transfer of glucose through the placenta, thereby
stimulating the release of insulin by fetal b-cells, which can
lead subsequently to increased fetal insulin secretion and
macrosomia [15]. This hypothesis was later extended,
suggesting that maternal amino acids and lipid substrates
are also important components relating to fetal growth [16].
Today, several studies support the association between
GDM and long-term health outcomes in the offspring. Luo
et al. [17] showed that maternal glucose intolerance in
pregnancy impairs fetal insulin sensitivity and thereby
programmes the susceptibility to Type 2 diabetes. Long-
term follow-up studies in groups of offspring of women with
GDM indicate that the offspring are more likely to be
overall and centrally obese, and to exhibit insulin resistance
and glucose intolerance in early adulthood [18]. Specifically,
Danish studies have shown that offspring (aged 18–
27 years) of women with GDM have an eight-fold higher
risk of Type 2 diabetes/prediabetes, a two-fold higher risk of
overweight and a five-fold higher risk of metabolic syndrome
than offspring from the background population [19,20].
Moreover, a recent study by Grunnet and colleagues [21],
including 600 offspring of mothers with GDM confirmed the
evidence of insulin resistance and obesity, and further
showed higher systolic blood pressure and an earlier onset
of puberty among the GDM female offspring compared with
control offspring.
Father
Although pregnancy may be considered a physiological
stressor unmasking predisposition to diseases such as Type
2 diabetes, and intrauterine exposure to hyperglycaemia
may programme disease susceptibility in the offspring, a
possible correlation between GDM and the health of the
father of the offspring may seem less clear. Yet, spouses
ª2018 Diabetes UK 715
Review article DIABETICMedicine
share common lifestyle factors and living conditions, and
obesity –a major risk factor for diabetes –has been shown
to spread within social networks [22]. A systematic review
and meta-analysis of mainly cross-sectional studies demon-
strated that a spousal history of diabetes is associated with
a 26% increased diabetes risk [23]. To examine whether a
similar association is found for GDM, Dasgupta and
colleagues [24] carried out a retrospective cohort analysis
and found that diabetes incidence was 33% higher in men
with partners with GDM compared with men whose
partner did not have a history of GDM. The association
was attenuated to an 18% higher incidence when adjusting
for shared deprivation level and ethno-cultural background,
suggesting that the association was partly mediated by these
factors. It has also been demonstrated that the combination
of GDM and gestational hypertension in the mother further
increases the risk for incident diabetes in the father over
that association with GDM and gestational hypertension
alone [13].
In summary, existing evidence suggests that GDM is
associated with increased short- and long-term adverse
outcomes for the mother and her offspring, including future
Type 2 diabetes. Further, although the causal mechanisms
are uncertain, women’s partners appear to likewise be at
higher risk of Type 2 diabetes. In other words, although
GDM is a condition diagnosed in pregnant women, it has
implications (whether causal or merely correlations) for the
Type 2 diabetes risk of the whole family.
How does the family context influence
treatment, post-partum lifestyle and
follow-up in women diagnosed with GDM?
Reports from the Diabetes Prevention Program (DPP) show
that structured intensive intervention with lifestyle and/or
metformin may prevent or delay the onset of Type 2
diabetes in women with impaired glucose tolerance and
prior GDM [25,26]. However, sustainable changes in such
health behaviours are difficult and many women with GDM
do not follow the recommendations after delivery [27].
Given the highly elevated risk in this group, this seems a
missed opportunity for health promotion aimed at preven-
tion of Type 2 diabetes and other non-communicable
diseases during the life course, for not only the mother,
but the entire family. Several studies have investigated the
various factors that inhibit engagement in recommended
healthy behaviours among women with prior GDM [28–
35]. Parsons and colleagues [29] conducted a meta-analysis
of qualitative studies and revealed a broad categorization of
inhibiting factors grouped into three themes: diabetes
beliefs, family context and health services. Despite these
categories not being watertight, the distinction between the
three levels can be helpful in conceptualizing and identifying
potential facilitators for intervention programmes for the
prevention of Type 2 diabetes.
Diabetes beliefs
Diabetes beliefs encompass the woman’s understanding
about diabetes, including her perception of susceptibility.
The concept of susceptibility or risk perception is prominent
in theories and models of health behaviour change building
upon or incorporating the Health Belief Model [36] and has
also found its way into research on health behaviours in
women with prior GDM [27,37]. In a US study, Kim and
colleagues [37] found that only 16% of women with a
history of GDM believed themselves to be at high risk of
diabetes, and that those who perceived themselves to be at no
or slight risk were less likely to change behaviours. Quali-
tative studies have shed light on various perceptions about
susceptibility in this group. Some women appear to simply
not be aware of the long-term risk of Type 2 diabetes and/or
have the understanding that their condition –GDM –is now
over and done with; wherefore, there is no need to worry
about or contemplate future diabetes [33,38]. Others recall
being made aware of future risk but then experience a lack of
concern, attention and focus from the healthcare system and
providers after the delivery that is interpreted, at least by
some, as the risk being no cause for concern, worry or action
[33]. Finally, studies have also reported a high but deter-
ministic perception prevalent among women with a strong
family history of diabetes [32,34]. Jones and colleagues [34]
found that women with GDM and a strong family history of
diabetes noted that there was nothing they could do to
prevent themselves from getting diabetes. Synthesizing the
existing evidence thus suggests that the women’s perceptions
of their susceptibility to developing diabetes are not isolated
entities but are shaped and influenced by factors pertaining to
the family as well as the healthcare system structures and
personnel.
The family context
The Health Belief Model states that perceived susceptibility is
an important component in understanding health behaviour
and suggests weighing up the potential costs and benefits of
engaging in a behaviour as important [36]. Paying attention
to the costs of –or rather the barriers to –the behaviour is
thus vital. In studies of women with prior GDM, several
barriers have been documented, especially in the family
context. Many of these pertain to everyday circumstances
with a baby or older child(ren). Feeling overwhelmed by the
demands of the baby and a lack of energy and time have been
highlighted as important barriers in several studies
[28,30,31,35]. Having support in terms of taking care of
the child(ren), as well as practical support with domestic
chores are therefore key for maintenance of the recom-
mended dietary and exercise behaviours [28,30,35,39].
However, social isolation and lack of motivation have also
been noted as barriers to a healthy lifestyle after a GDM-
affected pregnancy [28,30,35]. Social and emotional support
716 ª2018 Diabetes UK
DIABETICMedicine Prevention of diabetes after GDM in the family context K. K. Nielsen et al.
from a partner, family and friends to sustain motivation are
thus critically important [31,39]. Finally, the cost of a
healthy lifestyle whether in terms of, for example, buying
healthy food items or gym memberships has been given as a
barrier in some studies [28,31,35]. Prioritizing a healthy
lifestyle in everyday life within the family context whether in
time, psychosocial, practical or financial terms is thus a vital
challenge that needs to be addressed if delay or prevention of
future Type 2 diabetes is to occur. Yet, such prioritization is
influenced by the family’s diabetes beliefs as well as factors in
the healthcare system.
Another point for targeting prevention in a family context
is breastfeeding. Because previous studies have shown that
breastfeeding is associated with a reduced risk of developing
diabetes in mothers with previous GDM [40], increased
awareness and promotion of breastfeeding may reduce the
risk for diabetes later. Furthermore, the consequences of
gaining weight between pregnancies on outcomes (GDM and
others) in a new pregnancy are also very important within
the context of GDM women and future prevention of Type 2
diabetes. Previous large population-based cohort studies
have shown an association between an increase in interpreg-
nancy weight gain and the risk of adverse pregnancy
outcomes in the following pregnancy [41] and adverse
perinatal complications even in normal or underweight
women [42]. Additionally, a recent study showed that the
risk of developing GDM increased with increasing weight
gain from first to second pregnancy mostly in women with
BMI <25 in the first pregnancy [43]. Thus, weight retention
is indeed an important aspect within the context of preven-
tion of later diseases and complications both for the mother
and the offspring.
The healthcare system
In the healthcare system, women with GDM usually move
from being followed systematically by teams of nurses,
obstetricians, endocrinologists and dieticians during their
pregnancy to more sporadic (if any) follow-up in general
practice after pregnancy. Several studies have investigated
the process of Type 2 diabetes testing after pregnancy and
counselling of women with prior GDM in the healthcare
system and shown that this follow-up does not occur
routinely; that women with prior GDM find the received
information on risks and recommendations inadequate; that
care is not tailored to individual needs and preferences; and
that coordination of services and responsibility is often
unclear or lacking [31,44,45]. Thus, fragmentation of care,
lack of knowledge, as well as individualized counselling and
education result in missed opportunities for prevention and
early detection of Type 2 diabetes.
In summary, although evidence suggests that structured
lifestyle intervention may prevent or delay the onset of Type
2 diabetes in this target group, numerous challenges are
present when such efforts are sought implemented and
sustained in real-world settings and everyday life. Barriers to
maintaining a healthy lifestyle post-partum can be grouped
into pertaining to diabetes beliefs, the family context and the
healthcare system. Importantly, however, these tend to be
interlinked and interacting, and thus need to be addressed in
a comprehensive and multifaceted way.
What are potential avenues for future
research and practice?
Although evidence is accumulating on the short- and long-
term adverse health outcomes among members of GDM-
affected families and on the various barriers to the future
prevention of Type 2 diabetes, it remains unclear how best to
address these issues. There is a need to identify the best
avenue for evident health services and health promotion
planning. Current evidence shows many gaps in knowledge,
methodological limitations and questions left unanswered.
For example, can intervention during and after pregnancy
diminish the detrimental effect of hyperglycaemia in off-
spring? The few randomized control trials on treatment of
GDM examining potential long-term health benefits for the
offspring are not convincing with regards to long-term
impact, raising questions such as: is the glucose treatment
target too high; is treatment initiated too late; and/or is
glucose actually the wrong target in order to obtain a
beneficial health impact for the offspring? Also, although the
DPP studies suggested that Type 2 diabetes can be prevented
or at least delayed in women with prior GDM, the women
with prior GDM were enrolled in the DPP intervention with
a mean 12-year interval since the delivery of the index GDM
pregnancy, thus excluding women with prior GDM experi-
encing early conversion to Type 2 diabetes [26]. As Kim and
colleagues [10] showed, because the cumulative incidence of
Type 2 diabetes increases in the first 5 years after the GDM-
affected pregnancy, identifying effective prevention strategies
in the post-partum period is clearly a priority. The results of
a recent systematic review [46], however, indicate that much
remains to be understood about what such strategies should
involve if they are to be effective. Understanding the role of
biological, social and behavioural factors as well as their
potential interaction in the causal pathways to Type 2
diabetes incidence is of particular importance.
Nevertheless, health promotion focusing on not only
physical, but also social and psychological health and well-
being proposes potential avenues and approaches for pre-
vention in this target group. Health promotion and disease
prevention programmes often address the social determi-
nants of health, such as health literacy, which influence
modifiable risk behaviours. A core principle for health
promotion is the involvement of the target group and using
participation to ensure ownership and relevance from the
perspective of the target group(s). This is particularly
relevant in the design phase of interventions, but also during
implementation of Type 2 diabetes prevention efforts. Yet,
ª2018 Diabetes UK 717
Review article DIABETICMedicine
the target group may have to be considered in terms less
narrow than merely women with prior GDM. Dasgupta and
colleagues [39] carried out focus groups to study how to
optimize participation in diabetes prevention programmes
following GDM. One of the main outcomes from these
discussions was that direct participation of partners/spouses
in a diabetes prevention programme was viewed as impor-
tant to enhance support for behavioural change at home [39].
Of note, favourable impacts on offspring health were also
identified as a key motivator for health behaviour change in
this study. A recent intervention study from the UK and
Canada by McManus and colleagues [47] focused on healthy
living messages post-partum and included data on the
women’s partners. The study suffered from sizeable study
refusal and loss to follow-up, and at 12 months’ post-partum
there was no difference in weight loss. Yet, predictors for
completing the study’s 12-month follow-up included having
a partner involved in the study, and paternal weight was
found to be significantly correlated with maternal and
offspring weight [47]. Involvement of the father may thus
be relevant as well –not only to address his risk of Type 2
diabetes as previously described, but also as a source of social
support for the woman and in creating a healthy family
context.
Problems with study refusal, loss to follow-up and
sustainability of recommended healthy behaviours are a
key challenge in health promotion and research efforts
among women with prior GDM. Women with GDM
constitute a diverse group with characteristics such as age,
BMI and ethnicity being important risk factors. Conse-
quently, a one-size-fits-all approach may fall short, especially
considering the importance of long-term integration of
healthy behaviours to reduce the risk of Type 2 diabetes.
Rather, tailored or personalized approaches may hold
promise for long-term sustainability. Qualitative studies
from various countries have highlighted the importance of
culturally appropriate diet recommendations for women
from ethnic minority groups [33,34,38]. Furthermore, the
Australian MAGDA study by O’Reilly and colleagues
experienced substantial issues with recruitment and retention
in their intervention trial focusing on individual and group-
based sessions for women with prior GDM [48]. Engagement
of women during the first year after birth was a significant
challenge. Consequently, a second component offering tele-
coaching was tested, improving engagement in those not
engaging in the group-delivered component [49].
To address and mitigate the various barriers at the three
levels it may be particularly important to focus on health
literacy and risk perceptions. Health literacy is a critical
determinant of health and has been shown to be related to
health behaviour in people with diabetes. Within the
healthcare system, health literacy influences the interaction
between factors related to patients and factors related to the
system [50]. Addressing health literacy among women with
prior GDM may therefore be an important factor in ensuring
empowerment and behaviour change as well as access and
utilization of health care. As described earlier, studies suggest
that various risk perceptions are at play among women with
prior GDM; yet, limited evidence is available on what
influences these risk perceptions, their trajectories, and how
they may be altered. Although studies indicate that women
with GDM are highly motivated for behaviour change during
pregnancy due to the potential risk of hyperglycaemia on
their baby, motivation tends to cease after the delivery,
particularly due to factors within the family and healthcare
system [30,31,43]. Given the strong motivational drive for
behaviour change attached to the well-being of the offspring,
focusing on how parental behaviour affects that of their
children and thus their health may be a potential avenue for
enhancing motivation for healthy behaviours post-partum.
Importantly however, such efforts need to be carried out in
ways that are sensitive to not assigning blame to the mother
with GDM and inducing stigmatization and medicalization.
In summary, there is a need to identify effective approaches
to health services delivery and health promotion for the
women with prior GDM and their families. Future efforts
should ensure the involvement of the target group in the
planning, development and execution of such initiatives;
while also ensure that approaches are tailored to the needs of
the individual women and families, including in terms of
health literacy level and perceptions of health and disease
risk.
Funding sources
The symposium on which this review is based was funded by
the Danish Diabetes Academy, Odense, Denmark through a
grant from the Novo Nordisk Foundation. KKN and LGG
are funded by the Danish Diabetes Academy, which is
supported by the Novo Nordisk Foundation.
Competing interests
None declared.
Acknowledgements
We would like to thank the Danish Diabetes Academy,
which funded the symposium “What happens after GDM
pregnancy? –Perspectives on prevention of Type 2 diabetes
in a family, life-course and health systems perspective”, and
the organizing committee. We also thank the speakers in the
symposium, who all contributed in the preparation of this
review, and the participants in the symposium. Speakers and
members of the organizing committee at the DDA sympo-
sium who contributed to the manuscript: H. David McIntyre,
University of Queensland, Australia; Kaberi Dasgupta,
McGill University, Canada; Sharleen O’Reilly, Deakin
University, Australia and University College Dublin, Ireland;
Peter Damm, Center for Pregnant Women with Diabetes,
718 ª2018 Diabetes UK
DIABETICMedicine Prevention of diabetes after GDM in the family context K. K. Nielsen et al.
Dept. of Obstetrics, Rigshospitalet, Denmark; Dorte Møller
Jensen, Odense University Hospital, Denmark; Anne Timm,
Steno Diabetes Center Copenhagen, Denmark; Per Ovesen,
Aarhus University Hospital, Denmark; Christina Anne Vin-
ter, Odense University Hospital, Denmark; Jette Kolding
Kristensen, Aalborg University, Denmark; Jens Aagaard-
Hansen, Steno Diabetes Center Copenhagen, Denmark.
References
1 American Diabetes Association. 2. Classification and Diagnosis of
Diabetes. Diabetes Care 2017; 40(Suppl 1): S11–S24.
2 International Diabetes Federation. IDF Diabetes Atlas - 7th
Edition. Brussels: IDF, 2015.
3 Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med
Bull 2001; 60:5–20.
4 Barres R, Zierath JR. The role of diet and exercise in the
transgenerational epigenetic landscape of T2DM. Nat Rev Endo-
crinol 2016; 12: 441–451.
5 Pachucki MA, Jacques PF, Christakis NA. Social network concor-
dance in food choice among spouses, friends, and siblings. Am J
Public Health 2011; 101: 2170–2177.
6 Sonneville KR, Rifas-Shiman SL, Kleinman KP, Gortmaker SL,
Gillman MW, Taveras EM. Associations of obesogenic behaviors in
mothers and obese children participating in a randomized trial.
Obesity (Silver Spring) 2012; 20: 1449–1454.
7 HAPO Study Cooperative Research Group, Metzger BE, Lowe
LP, Dyer AR, Trimble ER, Chaovarindr U et al. Hyperglycemia
and adverse pregnancy outcomes. N Engl J Med 2008; 358:
1991–2002.
8 Black MH, Sacks DA, Xiang AH, Lawrence JM. Clinical outcomes
of pregnancies complicated by mild gestational diabetes mellitus
differ by combinations of abnormal oral glucose tolerance test
values. Diabetes Care 2010; 33: 2524–2530.
9 Kim C, Berger DK, Chamany S. Recurrence of gestational diabetes
mellitus: a systematic review. Diabetes Care 2007; 30: 1314–1319.
10 Kim C, Newton KM, Knopp RH. Gestational diabetes and the
incidence of type 2 diabetes: a systematic review. Diabetes Care
2002; 25: 1862–1868.
11 Bellamy L, Casas JP, Hingorani AD, Williams D. Type 2 diabetes
mellitus after gestational diabetes: a systematic review and meta-
analysis. Lancet 2009; 373: 1773–1779.
12 Shah BR, Retnakaran R, Booth GL. Increased risk of cardiovas-
cular disease in young women following gestational diabetes
mellitus. Diabetes Care 2008; 31: 1668–1669.
13 Pace R, Brazeau A-S, Meltzer S, Rahme E, Dasgupta K. Conjoint
associations of gestational diabetes and hypertension with diabetes,
hypertension, and cardiovascular disease in parents: a retrospective
cohort study. Am J Epidemiol 2017; 186: 1115–1124.
14 Ozanne SE, Constancia M. Mechanisms of disease: the develop-
mental origins of disease and the role of the epigenotype. Nat Clin
Pract Endocrinol Metab 2007; 3: 539–546.
15 Pedersen J. Diabetes And Pregnancy: Blood Sugar of Newborn
Infants. PhD thesis. Copenhagen: Danish Science Press, 1952.
16 Freinkel N. Banting Lecture 1980. Of pregnancy and progeny.
Diabetes 1980; 29: 1023–1035.
17 Luo ZC, Delvin E, Fraser WD, Audibert F, Deal CI, Julien P et al.
Maternal glucose tolerance in pregnancy affects fetal insulin
sensitivity. Diabetes Care 2010; 33: 2055–2061.
18 Metzger BE. Long-term outcomes in mothers diagnosed with
gestational diabetes mellitus and their offspring. Clin Obstet
Gynecol 2007; 50: 972–979.
19 Clausen TD, Mathiesen ER, Hansen T, Pedersen O, Jensen DM,
Lauenborg J et al. High prevalence of type 2 diabetes and pre-
diabetes in adult offspring of women with gestational diabetes
mellitus or type 1 diabetes: the role of intrauterine hyperglycemia.
Diabetes Care 2008; 31: 340–346.
20 Clausen TD, Mathiesen ER, Hansen T, Pedersen O, Jensen DM,
Lauenborg J et al. Overweight and the metabolic syndrome in
adult offspring of women with diet-treated gestational diabetes
mellitus or type 1 diabetes. J Clin Endocrinol Metab 2009; 94:
2464–2470.
21 Grunnet LG, Hansen S, Hjort L, Madsen CM, Kampmann FB,
Thuesen ACB et al. Adiposity, dysmetabolic traits and earlier onset
of female puberty in adolescent offspring of women with gesta-
tional diabetes mellitus: a clinical study within the Danish National
Birth Cohort. Diabetes Care 2017; 40: 1746–1755.
22 Christakis NA, Fowler JH. The spread of obesity in a large social
network over 32 years. N Engl J Med 2007; 357: 370–379.
23 Leong A, Rahme E, Dasgupta K. Spousal diabetes as a diabetes risk
factor: a systematic review and meta-analysis. BMC Med 2014; 12:
12.
24 Dasgupta K, Ross N, Meltzer S, Da Costa D, Nakhla M, Habel Y
et al. Gestational diabetes mellitus in mothers as a diabetes
predictor in fathers: a retrospective cohort analysis. Diabetes Care
2015; 38: e130–e131.
25 Aroda VR, Christophi CA, Edelstein SL, Zhang P, Herman WH,
Barrett-Connor E et al. The effect of lifestyle intervention and
metformin on preventing or delaying diabetes among women with
and without gestational diabetes: the Diabetes Prevention Program
outcomes study 10-year follow-up. J Clin Endocrinol Metab 2015;
100: 1646–1653.
26 Ratner RE, Christophi CA, Metzger BE, Dabelea D, Bennett PH,
Pi-Sunyer X et al. Prevention of diabetes in women with a history of
gestational diabetes: effects of metformin and lifestyle interven-
tions. J Clin Endocrinol Metab 2008; 93: 4774–4779.
27 Stage E, Ronneby H, Damm P. Lifestyle change after gestational
diabetes. Diabetes Res Clin Pract 2004; 63:67–72.
28 Graco M, Garrard J, Jasper AE. Participation in physical activity:
perceptions of women with a previous history of gestational
diabetes mellitus. Health Promot J Austr 2009; 20:20–25.
29 Parsons J, Ismail K, Amiel S, Forbes A. Perceptions among women
with gestational diabetes. Qual Health Res 2014; 24: 575–585.
30 Razee H, van der Ploeg HP, Blignault I, Smith BJ, Bauman AE,
McLean M et al. Beliefs, barriers, social support, and environmen-
tal influences related to diabetes risk behaviours among women
with a history of gestational diabetes. Health Promot J Austr 2010;
21: 130–137.
31 Svensson L, Kragelund Nielsen K, Terkildsen Maindal H. What is
the postpartum experience of Danish women following gestational
diabetes? A qualitative exploration. Scand J Caring Sci; https://doi.
org/10.1111/scs/12506 [Epub ahead of print].
32 Lie ML, Hayes L, Lewis-Barned NJ, May C, White M, Bell R.
Preventing type 2 diabetes after gestational diabetes: women’s
experiences and implications for diabetes prevention interventions.
Diabet Med 2013; 30: 986–993.
33 Zulfiqar T, Lithander FE, Banwell C, Young R, Boisseau L, Ingle
Met al. Barriers to a healthy lifestyle post gestational-diabetes:
an Australian qualitative study. Women Birth 2017; 30: 319–
324.
34 Jones EJ, Appel SJ, Eaves YD, Moneyham L, Oster RA, Ovalle F.
Cardiometabolic risk, knowledge, risk perception, and self-efficacy
among American Indian women with previous gestational diabetes.
J Obstet Gynecol Neonatal Nurs 2012; 41: 246–257.
35 Nicklas JM, Zera CA, Seely EW, Abdul-Rahim ZS, Rudloff ND,
Levkoff SE. Identifying postpartum intervention approaches to
ª2018 Diabetes UK 719
Review article DIABETICMedicine
prevent type 2 diabetes in women with a history of gestational
diabetes. BMC Pregnancy Childbirth 2011; 11: 23.
36 Rosenstock IM, Strecher VJ, Becker MH. Social learning theory
and the Health Belief Model. Health Educ Q 1988; 15: 175–183.
37 Kim C, McEwen LN, Piette JD, Goewey J, Ferrara A, Walker EA.
Risk perception for diabetes among women with histories of
gestational diabetes mellitus. Diabetes Care 2007; 30: 2281–2286.
38 Draffin CR, Alderdice FA, McCance DR, Maresh M, Harper Md
Consultant Physician R, McSorley O et al. Exploring the needs,
concerns and knowledge of women diagnosed with gestational
diabetes: a qualitative study. Midwifery 2016; 40: 141–147.
39 Dasgupta K, Da Costa D, Pillay S, De Civita M, Gougeon R, Leong
Aet al. Strategies to optimize participation in diabetes prevention
programs following gestational diabetes: a focus group study. PLoS
One 2013; 8: e67878.
40 Gunderson EP, Hurston SR, Ning X, Lo JC, Crites Y, Walton D
et al. Lactation and progression to Type 2 diabetes mellitus after
gestational diabetes mellitus: a prospective cohort study. Ann
Intern Med 2015; 163: 889–898.
41 Villamor E, Cnattingius S. Interpregnancy weight change and risk
of adverse pregnancy outcomes: a population-based study. Lancet
2006; 368: 1164–1170.
42 Bogaerts A, Van den Bergh BR, Ameye L, Witters I, Martens E,
Timmerman D et al. Interpregnancy weight change and risk for
adverse perinatal outcome. Obstet Gynecol 2013; 122: 999–1009.
43 Sorbye LM, Skjaerven R, Klungsoyr K, Morken NH. Gestational
diabetes mellitus and interpregnancy weight change: a population-
based cohort study. PLoS Med 2017; 14: e1002367.
44 Nielsen JH, Olesen CR, Kristiansen TM, Bak CK, Overgaard
C. Reasons for women’s non-participation in follow-up screen-
ing after gestational diabetes. Women Birth 2015; 28: e157–
e163.
45 Olesen CR, Nielsen JH, Mortensen RN, Boggild H, Torp-Pedersen
C, Overgaard C. Associations between follow-up screening after
gestational diabetes and early detection of diabetes –a register
based study. BMC Public Health 2014; 14: 841.
46 Pedersen ALW, Terkildsen Maindal H, Juul L. How to prevent type
2 diabetes in women with previous gestational diabetes? A
systematic review of behavioural interventions. Prim Care Diabetes
2017; 11: 403–413.
47 McManus R, Miller D, Mottola M, Giroux I, Donovan L. Trans-
lating healthy living messages to postpartum women and their
partners after gestational diabetes (GDM): body habitus, A1c,
lifestyle habits, and program engagement results from the Families
Defeating Diabetes (FDD) randomized trial. Am J Health Promot
2017; https://doi.org/10.1177/0890117117738210 [Epub ahead of
print].
48 O’Reilly SL, Dunbar JA, Versace V, Janus E, Best JD, Carter R
et al. Mothers after Gestational Diabetes in Australia (MAGDA): a
randomised controlled trial of a postnatal diabetes prevention
program. PLoS Med 2016; 13: e1002092.
49 Lim S, Dunbar JA, Versace VL, Janus E, Wildey C, Skinner T et al.
Comparing a telephone- and a group-delivered diabetes prevention
program: characteristics of engaged and non-engaged postpartum
mothers with a history of gestational diabetes. Diabetes Res Clin
Pract 2017; 126: 254–262.
50 Paasche-Orlow MK, Wolf MS. The causal pathways linking health
literacy to health outcomes. Am J Health Behav 2007; 31(Suppl 1):
S19–S26.
720 ª2018 Diabetes UK
DIABETICMedicine Prevention of diabetes after GDM in the family context K. K. Nielsen et al.