Depression and diabetes 2 The link between depression and diabetes: the search for shared mechanisms

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1 Depression and diabetes 2 The link between depression and diabetes: the search for shared mechanisms Calum D Moulton, John C Pickup, Khalida Ismail Depression is twice as common in people with type 1 or type 2 diabetes as in the general population, and is associated with poor outcomes. Evidence is growing that depression and type 2 diabetes share biological origins, particularly overactivation of innate immunity leading to a cytokine-mediated inflammatory response, and potentially through dysregulation of the hypothalamic-pituitary-adrenal axis. Throughout the life course, these pathways can lead to insulin resistance, cardiovascular disease, depression, increased risk of type 2 diabetes, and increased mortality. Proinflammatory cytokines might directly affect the brain, causing depressive symptoms. In type 1 diabetes, mediators of depression are not well studied, with research hindered by inconsistent definitions of depression and scarcity of observational, mechanistic, and interventional research along the life course. Despite few studies, evidence suggests that familial relationships and burden of a lifelong disorder with an onset early in personality development might contribute to increased vulnerability to depression. Overall, longitudinal research is needed to identify risk factors and mechanisms for depression in patients with diabetes, particularly early in the life course. Ultimately, improved understanding of shared origins of depression and diabetes could provide the potential to treat and improve outcomes of both disorders simultaneously. These shared origins are targets for primary prevention of type 2 diabetes. Introduction An association between depression and diabetes was recognised as early as the 17th century, when British physician Thomas Willis noted that diabetes frequently appeared in individuals who had experienced previous life stresses or sadness. 1 We now know that prevalence of depression in patients with type 1 or type 2 diabetes is about twice that of the general population without diabetes. 2 Both type 1 and type 2 diabetes result in persistent hyperglycaemia, but show important differences in their association with depression, which suggests that the association between each type might be driven by different underlying mechanisms. A bidirectional relation exists between type 2 diabetes and depression, and evidence is growing for biological correlates of depression in patients with type 2 diabetes, but less research into biological mechanisms for depression in patients with type 1 diabetes has been done. The two disorders typically occur at different ages and need different management. Type 1 diabetes presents characteristically in childhood and early adulthood, at a time of rapid psychological and physiological change, whereas type 2 diabetes typically occurs later, in mid-adulthood. Treatment of type 2 diabetes includes diet and lifestyle modification, and oral medication or insulin injections, whereas type 1 diabetes necessitates daily insulin injections or infusions for life. Additionally, average age of onset of depression early-to-mid-20s 3 suggests that important differences exist in its relation with type 1 and type 2 diabetes. We therefore discuss type 1 and type 2 diabetes separately in terms of their association with depression. The gold standard to diagnose depression is a diagnostic interview based on established diagnostic criteria, such as the Schedules of Clinical Assessment in Neuropsychiatry. 4 Much research into both type 1 and type 2 diabetes has instead used self-report questionnaires, sometimes with a cutoff to define depression or to describe depressive symptoms. Results of validation studies in patients with diabetes have shown that self-report questionnaires can substantially overdiagnose clinical depression. 5 However, whether the phenotype of depression in diabetes differs, at least in some patients, from depression in the non-diabetic population is not known. For example, biological symptoms of depression (eg, fatigue, and sleep and appetite disturbance) are often reported in patients with diabetes who do not meet criteria for clinical depression according to a diagnostic interview. 5 We therefore include papers that use both conventional diagnostic criteria and questionnaires to define depression. The related construct of diabetes-specific distress refers to emotional responses to diabetes, its treatment, and its effects on lifestyle and the future. 6 Although diabetesspecific distress has moderate-to-strong positive correlations with self-report measures of depression, much of the variance in diabetes-specific distress is unexplained. 6 Diabetes-specific emotional distress has been suggested to be a separate psychological construct to depression, and here we regard it as a potential mediator of the association between depression and diabetes self-management. Type 2 diabetes Overview One interpretation for the link between depression and type 2 diabetes is that the psychological burden of life with a chronic disorder predisposes patients to Lancet Diabetes Endocrinol 2015; 3: Published Online May 18, S (15) This is the second paper in a Series of three papers about depression and diabetes Department of Psychological Medicine, Institute of Psychiatry (C D Moulton MRCPsych, Prof K Ismail PhD) and Diabetes and Nutritional Sciences Division (Prof J C Pickup DPhil), King s College London, London, UK Correspondence to: Dr Calum D Moulton, Department of Psychological Medicine, Institute of Psychiatry, King s College London, London SE5 9RJ, UK calum.moulton@kcl.ac.uk Vol 3 June /05/ :23:40

2 depression, and depression in patients with type 2 diabetes is associated with poor self-care behaviours. 7 To support this interpretation, risk of depression seems to be higher in people with a diagnosis of type 2 diabetes than in people with impaired glucose metabolism or undiagnosed diabetes. 8 Another explanation is that depression is coincidental with type 2 diabetes because they share similar environmental and lifestyle factors, such as socioeconomic deprivation, social adversity, smoking, and reduced physical activity. For example, childhood adversity (abuse, deprivation, and neglect) has been shown to have effects on depression 9 and selfreported diabetes onset 10 in later life. In adulthood, work stress is associated with increased risk of type 2 diabetes 11 and depression. 12 Additionally, depression typically presents in early adult life and is linked to selfneglect and low self-esteem, which might increase risk of unhealthy lifestyles and, in turn, increase risk of type 2 diabetes. For example, depressive symptoms are associated with high body-mass index (BMI), poor diet, low levels of physical activity, and smoking, all of which are risk factors for type 2 diabetes and cardiovascular disease. 13 The cognitive behavioural model (figure 1) suggests that the burden of type 2 diabetes leads to low mood and negative thoughts about diabetes, which worsen diabetes self-care. Such negative thoughts and behaviours can be identified and modified with cognitive behavioural therapy (CBT) (figure 1), which slightly improves mood and glycaemic control in patients with type 2 diabetes. 14 Although glycaemic control tends to improve when treatment for depression is integrated with type 2 diabetes management, treatment of depression alone does not consistently improve glycaemic control. 15,16 Results of cross-sectional studies have shown a modest association between depression and high concentrations of haemoglobin A 1c (HbA 1c ). 17 However, prospective studies which are few in number have had mixed results, despite the more consistent finding that depression is a strong risk factor for macrovascular complications and dementia in patients with type 2 diabetes. 21,22 Evidence suggests that diabetes-related distress, rather than depression, is associated with decreased glycaemic control over time. 18 Moreover, the link between depression and type 2 diabetes is bidirectional: type 2 diabetes is associated with a roughly 20% increased risk of incident depression, 23,24 and depression is associated with a 60% increased risk of incident type 2 diabetes. 24 Collectively, these findings suggest that the relation between depression and type 2 diabetes is complex and that, in some individuals, shared biological mechanisms might underlie the association between, and the course of, depression and type 2 diabetes. Several biological mechanisms have been proposed for the association between diabetes and depression throughout the life course. Depression and diabetes have a moderate genetic correlation of r=0 19 (albeit with a broad CI of ), 25 whereas various type 2 diabetesrelated single nucleotide polymorphisms have been associated with depression and type 2 diabetes independently. 26,27 Preliminary evidence suggests that adaptations to the in-utero environment could drive socalled metabolic ageing and predispose patients to depression, potentially via epigenetic mechanisms such as DNA methylation marks. 28 Low birthweight followed by accelerated weight gain in childhood has large effects on incidence of type 2 diabetes in later life, 29 and a metaanalysis 30 showed a statistically significant association between low birthweight and later depression. Overall, these findings suggest that depression and type 2 diabetes could develop in parallel through shared biological pathways. Key candidate pathways include the innate inflammatory response, the hypothalamicpituitary-adrenal (HPA) axis, circadian rhythms, and insulin resistance, which all interact with each other. Although physiologically related and not mutually exclusive, we discuss these pathways separately for ease. Innate immunity and inflammation Activated innate immunity and an acute-phase inflammatory response are implicated in pathogenesis of type 2 diabetes. Specifically, raised concentrations of proinflammatory cytokines lead to pancreatic β-cell apoptosis and insulin resistance, and predict onset of type 2 diabetes in initially non-diabetic patients. 31 The importance of innate immunity in inflammation in type 2 diabetes has been substantiated by systematic reviews of prospective studies. 32 Additionally, anti-inflammatory agents, such as interleukin 1 receptor antagonist and nonsteroidal anti-inflammatory drugs, improve glycaemic control in placebo-controlled trials. 33,34 Growing evidence likewise suggests that the cytokine-mediated inflammatory response is associated with depression in people without diabetes. Increased cytokine serum concentrations activate the HPA axis, increase oxidative stress in the brain, and might activate the tryptophan kynurenine pathway, resulting in reduced production of serotonin. 35,36 Depressive symptoms and cognitive deficits are often reported in patients treated with the cytokine interferon alfa. 36 A meta-analysis of the association between cytokines and major depression reported that patients with depression had statistically significantly higher circulating concentrations of tumour necrosis factor (TNF) and interleukin 6 than those without depression. 37 Furthermore, a meta-analysis of four studies reported that adjunctive therapy with the PTGS2 inhibitor celecoxib reduced depressive symptoms. 38 However, participant numbers in these studies were low, and PTGS2 inhibitors are likely to be more problematic in patients with type 2 diabetes because they are associated with increased risk of thrombosis. 39 Although strong evidence implicates the innate immune system in the pathogenesis of depression in Vol 3 June /05/ :23:41

3 Core belief I don t care about diabetes Dysfunctional assumptions If I need insulin, that s the beginning of the end If I control my sugars, I ll get complications anyway Cognitive restructuring I can control the diabetes, not the diabetes control me It is in my power to slow complications down Situation Not taking medication as prescribed Not adhering to diet and lifestyle advice Behavioural experiments Try smaller portions of food Increase amount of walking Check blood sugar more frequently Altered cognition I am a failure I can t do anything about this Altered emotion Anxiety, depression, guilt, shame Physical symptoms Fatigue, dizziness Figure 1: Cognitive behavioural formulation for the link between depression and type 2 diabetes A core belief (an absolute statement about diabetes) leads to development of dysfunctional assumptions (rules that guide daily actions and expectations of diabetes management), which in turn leads to problems with management of diabetes. Problem situations in turn lead to negative emotions, physical symptoms, and negative thoughts, which interact with each other, generating a cognitive behavioural cycle. The dashed lines represent two techniques used in cognitive behavioural therapy that aim to break this cycle and thereby improve mood and glycaemic control: cognitive restructuring encourages patients to identify negative thoughts and assess evidence for and against them, to generate an objective view; and behavioural experiments are real-life activities done in or between sessions that might help to challenge negative thoughts, such as checking of blood glucose. the general population, only a minority of whom have diabetes, the role of innate immunity in development of depression in patients with type 2 diabetes is not yet established. In a primary-care sample of 1790 patients with newly diagnosed type 2 diabetes, patients with depression defined by a Patient Health Questionnaire 9 (PHQ-9) score of 10 or more were more overweight, younger, had higher concentrations of C-reactive protein (CRP) and interleukin 1-receptor antagonist, and higher white-cell counts than people with type 2 diabetes who were not depressed, even after adjustment for key covariates. 40 In other studies, increased concentrations of CRP and interleukin 6 predicted increased risk of type 2 diabetes 41 and depression 42 after adjustment for covariates. A large cohort study of 3573 patients with type 2 diabetes reported a statistically significant cross-sectional association between high CRP concentrations and depression, although after multivariate analysis, this association was shown only in patients with high BMI. 43 In the related specialty of cardiovascular disease, depressive symptoms predict high white-cell counts in patients with stable coronary heart disease, 44 and depression is an independent predictor of cardiovascular mortality after myocardial infarction. 45 Additionally, depression increases risk of incident dementia in patients with type 2 diabetes, 22 with increased concentrations of interleukin 6 associated with cognitive decline in patients with type 2 diabetes. 46 In epidemiological studies, innate immunity has been proposed as a possible mechanism by which depression and type 2 diabetes could develop as a result of stressors throughout the life course. In cross-sectional research, abuse, neglect, or both before age 16 years are major mediators of the cross-sectional relation between increased concentrations of inflammatory cytokines and depression in adults. 47 Cumulative exposure to low socioeconomic status from childhood to middle age is associated with increased risk of type 2 diabetes in adulthood, with interleukin 6 and CRP acting as independent predictors. 48 If inflammation is involved in pathogenesis of depression in type 2 diabetes, reduction in inflammation might be a novel treatment. However, no studies have attempted to modify inflammation in treatment of depression in patients with type 2 diabetes. With the potential benefit of improvement of glycaemic control and depressive symptoms concurrently, antiinflammatory approaches to treatment of depression in patients with type 2 diabetes are awaited. Vol 3 June /05/ :23:41

4 The HPA axis Stress is associated with activation of the HPA axis, which affects glucocorticoid production by the adrenal glands. Chronic stress with associated hypercortisolaemia can lead to increased portal and peripheral free fatty acids. 49 Additionally, hypercortisolaemia impairs the ability of insulin to translocate intracellular SLC2A4 glucose transporters to the cell surface. 50 Chronic hypercortisolaemia can therefore contribute to metabolic syndrome, insulin resistance, and type 2 diabetes. 51 Some evidence suggests that depression is associated with chronic dysregulation of the HPA axis. Excess cortisol hinders neurogenesis in the hippocampus, 52 a region implicated in both depression and type 2 diabetes. 53 Furthermore, patients with major depression show reduced expression of glucocorticoid-inducible genes TSC22D3 and SGK1, associated with smaller hippocampal volumes. 54 However, studies reporting overactivation of the HPA axis in patients with depression have often focused on inpatients or those with severe or melancholic subtypes, 55 whereas evidence for HPA-axis dysregulation in outpatients arguably most relevant for most people with depression and type 2 diabetes has been less convincing. 56,57 Nevertheless, the suggested role of HPA-axis dysregulation in both depression and type 2 diabetes provides a plausible common link between the two disorders throughout the life course. In the brain, early stress leads to attenuated development of the hippocampus and amygdala, areas that have a high density of glucocorticoid receptors and persistent postnatal neurogenesis 58 and that are implicated in both depression and type 2 diabetes. 53 Additionally, women with a history of childhood abuse have increased pituitary adrenal responses to stress compared with controls. 59 However, a study comparing features of the metabolic syndrome in healthy adult controls and adults with depression reported that depression is statistically significantly related with fasting glucose even in the absence of activation of the HPA axis. 60 If the HPA axis is associated with depression, pharmacological manipulation of the axis could provide novel treatments. Although mineralocorticoid antagonists prevented development of glucocorticoid-induced depressive behaviours in animals, 61 results of clinical studies have not shown improvement in depression with mineralocorticoid agonism or antagonism. 62 Moreover, the tendency for mineral ocorticoid antagonists, such as spironolactone, to worsen glycaemic control 63 emphasises the need for clear understanding of any shared aberrations of the HPA axis in depression and type 2 diabetes before pharmacological manipulation of the axis can provide safe and effective new treatments. Insulin resistance and secretion A positive association between depression and insulin resistance would increase plausibility of a biological link between depression and type 2 diabetes. A meta-analysis 64 of 21 studies investigating the link between depression and insulin resistance reported a small but statistically significant cross-sectional association, but this link was attenuated in analyses adjusted for bodyweight and other confounders. However, interpretation is limited by a scarcity of longitudinal data in this area; studies included in the meta-analysis used estimates of insulin resistance such as homoeostatic model assessment-insulin resistance (HOMA-IR), because the gold standard (the hyperinsulinaemic-euglycaemic clamp) is not practical for large-scale studies. One of the few prospective studies reported that depression was associated with high HOMA-IR values and incident diabetes in middle-aged women, mediated mostly through central adiposity. 65 A 6-year prospective study of adults aged years reported that somatic-vegetative symptoms of depression (fatigue, sleep disturbance, and appetite changes) were associated with worsened insulin resistance over time, partly mediated by increased BMI. 66 If association with depression is clinically significant, reduction of insulin resistance could be a potential treatment for depression, and could slow down development of type 2 diabetes at the same time. Pioglitazone, which reduces insulin resistance by stimulating the nuclear receptor PPARγ and, to a lesser extent, PPARα, has been shown to improve depressive symptoms in patients with bipolar depression, predicted by increased baseline concentrations of interleukin 6, 67 although this trial was uncontrolled. In a double-blind metformin-controlled trial, pioglitazone improved depressive symptoms compared with metformin. 68 Because both drugs increase sensitivity to insulin, no difference in HOMA-measured insulin resistance is expected, but other biological pathways are implicated in this effect. 68 However, because the study was undertaken in a population with polycystic ovarian syndrome, and patients with worsened depressive symptoms (Hamilton Depression Rating Scale >20) were excluded, these results should be treated with caution. Circadian rhythms Disruption of normal circadian rhythm is implicated in both depression 69 and type 2 diabetes. 70 Sleep apnoea, which is common in patients with type 2 diabetes, is associated with disruption of circadian rhythm. 70 Extremes of sleep duration have been shown in patients with depression 71 and metabolic syndrome, 72 and increased concentrations of CRP and interleukin 6 have been reported in long sleepers with depression. 71 Patients with depression and patients with type 2 diabetes have common variations in sleep architecture, such as decreased slow-wave sleep and increased rapid eye movement density, associated with increased concentrations of proinflammatory cytokines, such as interleukin 6 and TNF. 73 Such sleep architecture variations can be seen before onset of depressive Vol 3 June /05/ :23:41

5 symptoms, 74 suggesting that a subpopulation might be at increased risk of depressive symptoms and metabolic disturbances. At the cellular level, clock genes are associated with regulation of circadian rhythm, and their expression is controlled by environmental cues such as light dark cycles, food, and social cues. 75 In patients with type 2 diabetes, clock gene expression has been directly associated with fasting glucose concentrations. 76 In patients with depression, the rapid antidepressant actions of low-dose ketamine and sleep deprivation therapy might be due to resetting of abnormal clock genes and subsequent restoration of circadian rhythms. 77 This finding highlights the translational potential of these emerging biological pathways, and studies investigating the role of clock genes in depression in patients with type 2 diabetes are awaited. An alternative explanation: antidepressants rather than depression? Prescription of antidepressant medication, independently of depression itself, has been suggested as a possible link between depression and type 2 diabetes. One study 78 reported that a medication history of more than 200 defined daily doses of conventional antidepressants increased risk of diabetes in patients with moderate or severe depression by % compared with the general population. However, subsequent analysis by the same authors 79 suggested that the link was not causal. Selective serotonin reuptake inhibitors (SSRIs) improve glucose regulation in the short term in the general population, 80 and use of SSRIs for 1 year in patients with established type 2 diabetes is not associated with reduction of Environmental threats and toxins Obesity, sedentary lifestyle, smoking, and chronic social adversity Macrophages Pro-inflammatory cytokines (interleukin 6, interleukin 1, and TNF) causing sickness behaviours Acute-phase response Blood proteins (C-reactive protein; serum amyloid A) and triglycerides Cell damage Pancreatic β cells, insulin resistance, endothelial cells (arterial), and neuroglia (brain cells) Disease Type 2 diabetes, atherosclerosis, depression, and cognitive impairment Figure 2: Flow diagram showing the effects of the innate immune response after activation by toxins throughout the life course glycaemic control. 81 Because SSRIs are the most frequently prescribed antidepressants with known anorexigenic properties, 39 this finding suggests that they have no causal role in type 2 diabetes. Future research should identify clearly the prospective relation between baseline antidepressant use and development of prediabetes stages, and the extent to which antidepressant use has direct effects on diabetogenic metabolic pathways, rather than being a proxy marker of depression itself. Summary: depression and type 2 diabetes share biological origins Despite limitations in methodological quality of many studies, evidence of shared psychological and, increasingly, biological mechanisms for depression and type 2 diabetes is consistent. In some individuals, these shared mechanisms might lead to development of both disorders in parallel. Fetal or maternal stress in utero, cumulative exposure to low socioeconomic status, and poor health behaviours in people with a genetic predisposition might promote dysregulation of the HPA axis, promote disturbance of circadian rhythms, and act as toxins to activate the innate inflammatory response (figure 2). Dysregulation of these biological pathways might lead, in parallel, to insulin resistance and type 2 diabetes, depression, dementia, and cardiovascular disease. Depressive symptoms or depression might arise in patients with diabetes when excess proinflammatory cytokines in the brain lead to increased breakdown of tryptophan to neuroactive metabolites such as kynurenine, and reduced concentrations of serotonin (figure 3). Reasons why depression typically presents at a younger age than type 2 diabetes are not known. Possible hypotheses are that the brain is more sensitive to the end-effects of these biological pathways, or that the effect of environmental stress on the brain is the first event, which, in turn, affects central regulation of metabolism. Type 1 diabetes Overview Patients with type 1 diabetes need a complex management regimen, including regular and frequent monitoring and recording of blood glucose concentrations and calculation and administration of insulin doses in the context of carbohydrate intake and physical activity. People with type 1 diabetes might struggle to accept and adjust to this monitoring to different extents, posing a practical and psychological burden. The cognitive behavioural model is often used to explain the link between depression and type 1 diabetes (figure 4). In type 1 diabetes, CBT has been used to help patients to identify and reframe negative beliefs about their disease, which might otherwise result in overwhelming frustration and abandonment of self-care activities, such as selfmonitoring of blood glucose. 82 A systematic review 83 of patients with and without depression identified that psychological treatments, predominantly CBT, slightly Vol 3 June /05/ :23:42

6 Genetic factors Innate immunity and inflammation HPA axis dysregulation In-utero stress and nutrition Childhood adversity Unhealthy lifestyles Adulthood adversity Insulin resistance β-cell apoptosis Hippocampal atrophy Endothelial dysfunction Circadian rhythm disturbance Depression Type 2 diabetes Cardiovascular disease Dementia Figure 3: Summary of shared biological pathways contributing to pathogenesis of depression and type 2 diabetes throughout the life course HPA=hypothalamic-pituitary-adrenal. improved glycaemic control in patients with type 1 diabetes. However, results of an uncontrolled study of group CBT for depression showed reduced depression in the subgroup with type 1 diabetes, but no improvement in glycaemic control. 84 In addition to psychological mechanisms, biological mechanisms, such as inflammation and cerebral damage, might have a role in mediation of the link between depression and type 1 diabetes. 85 The role of biological pathways might be a barrier to conventional treatments for depression in patients with type 1 diabetes and, conversely, could be a new modifiable target for intervention. However, in a large-scale cohort study of children diagnosed with diabetes before age 20 years, only high concentrations of apolipoprotein B were associated with worsened depressive symptoms in patients with type 1 diabetes after adjustment for confounders. 86 Some authors have highlighted parallels in cerebral correlates for depression and type 1 diabetes. 85 However, although changes typical of depression, such as hippocampal atrophy, are consistently noted in patients with type 2 diabetes, the cerebral correlates of type 1 diabetes seem to be different, and only thalamic atrophy is a consistent finding. 53 Type 1 diabetes is characterised by a much earlier age of onset than type 2 diabetes, and has the potential to cause substantial disruption to normal developmental processes. Childhood Depression can be difficult to diagnose in childhood, and few studies have investigated the association between depression and type 1 diabetes during this period. Although some aspects of diabetes management might be done by the children themselves, such as selfadministration of insulin, the adult caregiver is mostly responsible for the complex decision making associated with these tasks, such as dosing insulin on the basis of blood glucose readings and diet. Therefore, the relation between depression and type 1 diabetes in childhood take into account both the child and their familial relationships. Some evidence suggests that children with type 1 diabetes who grow up in an environment of high expressed emotion have poor glycaemic control. 87 The burden of parental responsibility during childhood is a prominent theme of qualitative studies in patients with type 1 diabetes. 88 In children with type 1 diabetes, evidence suggests that critical parenting behaviours increase depressive symptoms, with associated reduction of self-care behaviours. 89 Clinically, addition of structured behavioural group training has been shown to reduce parental stress and, possibly, maintain improved glycaemic control over time. 90 Quality of attachment between child and parents or guardians is a plausible mediator of the child s adjustment to type 1 diabetes and subsequent psychological sequelae. Attachment theory proposes that past experiences with caregivers are incorporated psychologically to form cognitive models that inform future interpersonal relationships, and these patterns of attachment continue into later life. 91 Individual differences exist in the way that people regulate their attachment behaviour in response to threats, such as illness. In adults with type 1 diabetes, dismissing attachment style characterised by low trust of others and excessive self-reliance is associated with increased risk of poor glycaemic control. 92 However, studies examining attachment behaviour, psychological adjustment, and glycaemic control in children with type 1 diabetes are awaited. Adolescence The transition from childhood into adolescence necessitates increased independence and diabetes selfmanagement, such as self-monitoring of blood glucose, dietary intake, and insulin dosing, 93 behaviours with which depression has been shown to interact adversely. 94 This increased independence coincides with emergence of risk-taking behaviours, such as experimentation with tobacco and alcohol, and desire for peer approval. Additionally, onset of puberty results in decreased glucose uptake, owing in part to increased activity of the growth hormone axis. 95 In view of these rapid psychological and physiological changes, diabetes-specific distress is well characterised in adolescents with type 1 diabetes, and is associated with poor glycaemic control, prominent negative beliefs about diabetes, and reduced self-efficacy. 96 Fear of hypoglycaemia might result in increased anxiety, guilt, and avoidant behaviour. 97 Coping skills training in adolescents results in decreased HbA 1c concentrations and improved diabetes self-care and quality of life. 98 However, a meta-analysis of psychoeducational interventions reported that no programme has proven effective in randomised studies for patients with poor glycaemic control Vol 3 June /05/ :23:43

7 Core belief I hate having diabetes Dysfunctional assumptions If I check my sugars in public, people will think I am taking drugs If I have a hypo, it will be humiliating and no one will help me Cognitive restructuring I guess many people check their blood sugars I can control my sugars without necessarily having a hypo Behavioural experiments Checking blood sugar more frequently in private or public Gradually increasing insulin dose Situation Not checking blood sugar Omitting insulin Altered cognition I am a failure I don t want to think about this Altered emotion Anxiety, depression, guilt, shame Physical symptoms Fatigue, dizziness Figure 4: Cognitive behavioural formulation for the link between depression and type 1 diabetes As with type 2 diabetes, a core belief about type 1 diabetes leads to development of dysfunctional assumptions, which in turn lead to problems with management of type 1 diabetes. In this example, frequent difficulties with insulin management provide opportunities for therapeutic intervention (behavioural experiments and cognitive restructuring), thereby improving both mood and diabetes management. Additionally, type 1 diabetes in adolescence can lead to negative communication and difficulties within the wider family. Family stress is associated with poor glycaemic control in adolescents with type 1 diabetes, 100 and parental stress is a possible mediator of both adolescent depression and poor glycaemic control. 101 Adolescence is a key period for development of eating disorders, which are likewise associated with depression and the desire for peer approval. 102 Some prospective studies have investigated the association of eating disorders with depression and type 1 diabetes concomitantly, but the interaction is complex. In a casecontrol study comparing patients with both type 1 diabetes and an eating disorder with those with an eating disorder alone, the group with type 1 diabetes had statistically significantly lower scores on the Beck Depression Inventory an unexpected outcome. 103 Adolescents with type 1 diabetes and disturbed eating behaviour a generic term for subthreshold eating disorder symptoms are far more likely to report depressive symptoms than those with type 1 diabetes alone, but do not consistently have poorer glycaemic control prospectively. 104 Clinically, if adolescents with depression and type 1 diabetes develop poor diabetes outcomes or have high comorbidity, routine depression screening in patients with type 1 diabetes could improve outcomes. Results of a study of 528 adolescents with type 1 diabetes showed that high scores on the Children s Depression Inventory (CDI) were associated with decreased blood glucose monitoring frequency and increased HbA 1c concentrations. 105 However, in another study, prevalence of depressive symptoms as measured by the CDI in patients with poor glycaemic control was similar to prevalence in those with good glycaemic control. 106 These apparently conflicting findings might be due to differences in methods, since correlation between depression score and HbA 1c concentration 105 is more sensitive than bivariate comparison of high and low HbA 1c concentration in relation to depression score. 106 However, these findings highlight the need for longitudinal assessment of potential benefits of depression screening on type 1 diabetes outcomes, and emphasise the apparent vulnerability of all adolescents, irrespective of HbA 1c concentration, to development of depression. Adulthood Relative to the many studies of prevalence of depression in patients with type 1 diabetes in adulthood, mechanistic studies of depression have been sparse. A systematic review reported inconclusive evidence that prevalence of depressive symptoms is increased in young adults with type 1 diabetes, but showed that those who are most depressed have poorest glycaemic control. 107 However, cross-sectional evidence suggests that diabetes-specific emotional distress, rather than depression, is associated with poor glycaemic control in adults with type 1 Vol 3 June /05/ :23:43

8 Search strategy and selection criteria We searched PubMed from Jan 1, 1900, to Dec 18, 2014, for peer-reviewed articles only, with the keywords: diabetes, diabetic, depression, depressive, and distress. For different sections, these keywords were combined with the following: childhood, parent, parenting, attachment, adolescence, adolescent, adult, adulthood, adult-onset, inflammation, inflammatory, immune, HPA, cortisol, hypothalamic-pituitary-adrenal, genetic, genetics, in utero, uterine, birth, childhood, trauma, stress, anti-depressant, anti-depressants, insulin resistance, insulin sensitivity, insulin secretion, HOMA-IR, antidepressant, antidepressants, clock genes, clock gene, circadian, and sleep. We limited the searches to English languages articles and excluded case reports, commentaries, and letters. We also screened reference lists of included papers. Because of space constraints, we could not cite every paper of potential relevance. Of interventional studies, randomised trials were prioritised where possible. Of observational studies, meta-analyses and prospective studies received priority where possible. diabetes. 108 In a cross-sectional study of 6712 adults with type 1 diabetes, patients with depression were more likely to be of non-white ethnicity, to be of low socioeconomic status, to have poor glycaemic control, and to have increased numbers of diabetic complications, suggesting that social factors are neglected but relevant risk factors for poor diabetes control. 109 Little direct evidence exists for the cognitive behavioural model for depression in type 1 diabetes, but most psychological treatments to improve glycaemic control apply cognitive behavioural techniques with small but clinically significant effects. 84 Summary: link between depression and type 1 diabetes The consensus suggests that worsened depressive symptoms are noted in patients with type 1 diabetes, but whether these symptoms consistently correlate with poor glycaemic control is unclear, and understanding of mechanisms of depression in patients with type 1 diabetes is limited. The close chronological relation between type 1 diabetes and onset of depression is striking, with ongoing adjustment to diagnosis of type 1 diabetes and its treatment burden occurring at a time of increasing vulnerability to depression. Further research is needed to identify factors predicting depression, comparing biological (inflammation), psychological (family and individual), and environmental (schooling and social adversity) risk factors for depression in large population-based prospective cohorts of patients with type 1 diabetes, comparing them with healthy controls, with patients with other long-term disorders, or both, across the life course. Additionally, studies are needed to develop sophisticated psychological models of diabetes looking beyond CBT such as whether attachment theory might help to explain depression in patients with type 1 diabetes. Future directions In both type 1 and type 2 diabetes, greater understanding is needed of the similarities and differences between correlates of depressive symptoms, depression, and diabetes-specific distress. In type 1 diabetes, further research is needed to identify risk factors for depression, taking developmental stage into account, by use of systematic models of family dynamics, CBT, attachment theory, and key transition points in adolescence. Further research should investigate potential biological and cerebral correlates of depression in patients with type 1 diabetes, to elucidate potentially modifiable factors for treatment of depression in these patients. In type 2 diabetes, further basic science research, such as studies in animals, could identify clearly the concurrent effects of biological processes, both peripherally and centrally. Although consistent neuroimaging correlates of both type 2 diabetes and depression have been reported separately, almost no studies have investigated the two disorders together. Large, well characterised cohorts are needed to test whether shared origins of depression and type 2 diabetes exist at a genome-wide association significance level. At the same time, future research should examine the longitudinal relation between depression and prediabetes stages, which might provide opportunities for timely interventions to slow down or stop the course of diabetes, depression, or both. More research is needed to investigate depression and type 2 diabetes concurrently across the life course, and to identify clearly their temporal relation and biological correlates. Because most patients with depression do not develop type 2 diabetes, and vice versa, future research should identify biological characteristics of individuals at high risk of these disorders and associated complications. The further upstream that interventions target these shared biological pathways, the greater the clinical benefit will be. In established type 2 diabetes, for example, identification of biomarkers predicting macrovascular complications could delay or prevent their onset. Characterisation of biomarkers of depression in patients with type 2 diabetes could identify patients who might benefit from anti-inflammatory medications or other immune-modifying therapies. Most excitingly, identi fication and modification of upstream biomarkers of both depression and type 2 diabetes could, in some cases, wholly prevent development of these two chronic and debilitating disorders. Contributors CDM did the literature search and wrote the first draft. KI wrote the outline for the paper. JCP and KI revised the manuscript. All authors approved the final draft. Declaration of interests We declare no competing interests Vol 3 June /05/ :23:43

9 References 1 Willis T. Diabetes: A Medical Odyssey. Tuckahoe, New York: USV Pharmaceutical Corp, Anderson RJ, Freedland KE, Clouse RE, Lustman PJ. The prevalence of comorbid depression in adults with diabetes: a meta-analysis. Diabetes Care 2001; 24: Kessler RC, Amminger GP, Aguilar-Gaxiola S, Alonso J, Lee S, Ustün TB. Age of onset of mental disorders: a review of recent literature. Curr Opin Psychiatry 2007; 20: Wing JK, Babor T, Brugha T, et al. SCAN. Schedules for Clinical Assessment in Neuropsychiatry. Arch Gen Psychiatry 1990; 47: Twist K, Stahl D, Amiel SA, Thomas S, Winkley K, Ismail K. Comparison of depressive symptoms in type 2 diabetes using a two-stage survey design. Psychosom Med 2013; 75: Snoek FJ, Bremmer MA, Hermanns N. Constructs of depression and distress in diabetes: time for an appraisal. Lancet Diabetes Endocrinol 2015; published online May doi.org/ /s (15) Katon WJ, Russo JE, Heckbert SR, et al. The relationship between changes in depression symptoms and changes in health risk behaviors in patients with diabetes. Int J Geriatr Psychiatry 2010; 25: Nouwen A, Nefs G, Caramlau I, et al, and the European Depression in Diabetes Research Consortium. Prevalence of depression in individuals with impaired glucose metabolism or undiagnosed diabetes: a systematic review and meta-analysis of the European Depression in Diabetes (EDID) Research Consortium. Diabetes Care 2011; 34: Colman I, Jones PB, Kuh D, et al. Early development, stress and depression across the life course: pathways to depression in a national British birth cohort. Psychol Med 2014; 44: Scott KM, Von Korff M, Angermeyer MC, et al. Association of childhood adversities and early-onset mental disorders with adult-onset chronic physical conditions. Arch Gen Psychiatry 2011; 68: Heraclides A, Chandola T, Witte DR, Brunner EJ. 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