DIABETICMedicine DOI: 10.1111/dme.13622
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 Nielsen1,2,3 , L. Groth Grunnet2,3,4 and H. Terkildsen Maindal1,5 the Danish Diabetes Academy Workshop and Workshop Speakers
on behalf of
1 Health Promotion Research, Steno Diabetes Center Copenhagen, Gentofte, 2Department of Public Health, University of Copenhagen, Copenhagen, 3The Danish Diabetes Academy, Odense, 4Department of Endocrinology, Rigshospitalet, Copenhagen and 5Department 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, especially how these may be averted in real-life settings.
Correspondence to: Karoline Kragelund Nielsen. E-mail:
[email protected]
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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 intrauterine environment also impacts long-term health outcomes such as obesity, cardiovascular disease and diabetes [3]; wherefore, 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 people live their everyday lives is important for understanding
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why some people remain healthy while others develop diseases. The potential for Type 2 diabetes prevention after a GDMaffected 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 presentations 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 encountered 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 preeclampsia, gestational hypertension and caesarean section during pregnancy and delivery compared with their normoglycaemic 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 cardiovascular disease, and that the magnitude of the association
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increases sharply in combination with gestational hypertension [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 intrauterine 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 programmed 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 overnutrition – the latter by, for example, hyperglycaemia occurring at critical points during development – may induce permanent adaptive programming in key organs potentially mediated 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. Longterm 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 715
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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 demonstrated 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 prevention 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. 716
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. Qualitative 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 deterministic 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 recommended 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 GDMaffected pregnancy [28,30,35]. Social and emotional support
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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 interpregnancy 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 prevention 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
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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 longterm adverse health outcomes among members of GDMaffected 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 offspring? 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 experiencing 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 GDMaffected 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 wellbeing proposes potential avenues and approaches for prevention in this target group. Health promotion and disease prevention programmes often address the social determinants 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, 717
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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 important 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. Consequently, 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 groupbased 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 telecoaching 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 718
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 symposium 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,
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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 Vinter, Odense University Hospital, Denmark; Jette Kolding Kristensen, Aalborg University, Denmark; Jens AagaardHansen, Steno Diabetes Center Copenhagen, Denmark.
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