Introduction

The comorbidity between severe mental illnesses (SMI) and increased prevalence of type 2 diabetes mellitus (T2D) is well established in many different studies. Particularly, prevalence estimations of T2D among patients with schizophrenia in the European countries range from 11.3% in the UK [1] to 22% in a cross-sectional study in Finland [2]. Accordingly, T2D prevalence varies 1.7–3.2-fold higher [3,4,5,6,7] among patient populations with bipolar disorder in comparison with the general population, whereas factors such as female gender, age over 40, and obesity appear to have significant additional risk [7, 8]. Similarly, a retrospective analysis in the USA using the 2002–2014 Nationwide Inpatient Sample databases measured the rate of depression among patients with T2D to 15.4% in 2014, whereas prevalence reached 7.6% in 2002, respectively [9], reflecting also the increasing tendency.

Apart from common diabetogenic factors applying in the general population, such as smoking, hypertension, obesity, poor diet, limited physical activity, and hyperlipidemia, unique conditions attribute additionally on diabetes onset among individuals suffering from psychiatric problems. Specifically, the excessive sedentary lifestyle followed often by persons with SMI [10, 11], social determinants and the limited access to primary medical care [12] contribute to diabetes onset. Further, a shared genetic etiology is proposed for diabetes and mental illness co-occurrence, given the observed higher prevalence of diabetes in young patients, newly diagnosed with schizophrenia or bipolar disorder and treatment-naive [13,14,15, 16••]. Additionally, many psychiatric drug regiments are markedly considered responsible for increased the risk of diabetes and other metabolic disorders, though literature is not always consistent [17, 18].

Consideration of the increasing prescription of psychotropic medications, not only as required by official recommendations and therapeutic guidelines, but also as often applied off label, strengthens the need for deep knowledge of their potential diabetogenic side effects. Therefore, the purpose of this review is to clarify, according to literature search, not only the prospective relation of psychotropic substances use, and mainly first-generation antipsychotics (FGA), second-generation antipsychotics (SGA), antidepressants (AD), mood stabilizers (MD), with the development of diabetes, but also the extent to which their use has direct effects on diabetogenic metabolic pathways. A MEDLINE search was conducted via PubMed using in various combinations the following keywords: First Generation Antipsychotics, Second Generation Antipsychotics, Antidepressants, Mood stabilizers, anxiolytics, hypnotics, side effects, diabetes. Only English-language articles published from 1995 to 2017 were included and reviewed.

Antipsychotics

Second-generation antipsychotics (SGAs) represent the first line treatment for psychotic disorders. They present high affinity for dopamine D2 receptors in the mesolimbic pathway and serotonin receptors (particularly 5-hydroxy-tryptamine 2A receptor [5-HT2A], 5-hydroxy-tryptamine 2C receptor [5-HT2C], and 5-hydroxy-tryptamine 1A receptor [5-HT1A]), both regulating feeding behavior [19, 20], ranging from risperidone acting overwhelmingly on serotonin receptors, to amisulpride with no serotonergic activity. Therefore, they present with lower propensity to produce extrapyramidal side effects [20, 21]. However, the majority of SGAs are associated with significant weight gain and further T2D development [22,23,24] (Table 1). This is additionally due to their high affinity with Muscarinic M2 and M3 receptors, which are considered relevant for glucose homeostasis, controlling cholinergic-dependent insulin release [29,30,31,32,33]. FGAs are not particularly selective and block dopamine receptors in all of the pathways (mesolimbic, mesocortical, tuberoinfundibular, and nigrostriatal pathways) [34]. Finally, weak genetic evidence suggests association of antipsychotic induced weight gain with leptin, G-protein and promelanin-concentrating hormone signaling, as well with cannaboid receptor activity and a-adrenergic transmission [19, 35,36,37,38].

Table 1 Review of antipsychotic drug effects on diabetogenic risk and weight gain

Comparison between SGAs with first FGAs revealed a 1.3-folds elevated risk for diabetes [39], an effect intermediated either by weight gain, or in 25% of cases [40] though direct impairment in glucose homeostasis, potentially via blockade of central and peripheral M3 receptors [41, 42]. Similarly, another study revealed increased T2D risk for both patient groups treated with SGA (adjusted hazard ratio [HR] 1.32, 95% confidence intervals [CI] 1.01–1.75) or those under FGA treatment (adjusted HR 1.82, 95% CI 1.30–2.55) against control patients without schizophrenia and psychotropic medication [43]. Furthermore, a meta-analysis reported 2.1% T2D prevalence among antipsychotic-naïve patients, whereas the prevalence was 12.8% for antipsychotic receivers [44]. Nevertheless, a systematic review of 22 prospective, randomized, control trials, though short-term followed, detected no difference in glycemic abnormalities between placebo and antipsychotic cohorts [27].

Proposed explanations to those inconsistent findings are beyond methodological problems such as sample size, medication pre-exposure of tested groups, duration and dose of daily medication received, control for therapy adherence, severity, duration and type of psychiatric disorder, homogeneity of case group (schizophrenia, schizoaffective disorders, psychosis), way of diabetes diagnosis estimation (self-report, anti-diabetes drugs, American Diabetes Association (ADA) criteria) or the differences in metabolic traits measured such as homeostasis model insulin resistance (HOMA-IR), glycated hemoglobin A1c (HbA1c), fasting glucose, the follow-up period, but also other unobserved confounding factors, such as the unbalanced diet, the physical activity, the sleep duration, psychiatric disease severity. Notably, the heterogeneity inside each group of SGAs and FGAs potentially reflects differences in terms of diabetogenic effect.

Accordingly, other studies attempted to evaluate the diabetogenic role of each antipsychotic regiment separately. A large, population-based study conducted in Denmark with 345,937 cases treated with antipsychotics and 1,426,488 controls found 1.45% for clozapine, 1.29% for olanzapine, and 1.23% for risperidone, 1.94% for sertindole, 1.57% for perphenazine, 1.94% for ziprasidone, and even 1.17 for haloperidol increased diabetes risk [25], whereas no increase in diabetes risk was detected for aripiprazole, amisulpride or quetiapine. On the other hand, a study on newly-onset schizophrenia patients revealed diabetes incidence patients with olanzapine initiation therapy (hazard ratio, HR = 1.41) and with mid-potency conventional antipsychotics (HR = 1.60) [45]. Moreover, a Food and Drug Administration (FDA) database analysis on T2D onset, reported the following adjusted ratios hierarchy for diabetes-mellitus-related adverse outcomes: olanzapine 9.6 (95% CI 9.2–10.0), risperidone 3.8 (95% CI 3.5–4.1), quetiapine 3.5 (95% CI 3.2–3.9), clozapine 3.1 (95% CI 2.9–3.3), ziprasidone 2.4 (95% CI 2.0–2.9) aripiprazole 2.4 (95% CI 1.9–2.9) and haloperidol 2.0 (95% CI 1.7–2.3) [28]. Clozapine and olanzapine are consistently associated with greater weight gain risk. [46]. Among SGAs, clozapine and olanzapine are detected to have the higher risk for causing weight gain and glucose dysregulation, iloperidone, paliperidone, quetiapine, and risperidone a medium risk and aripiprazole, asenapine, lurasidone, and ziprasidone present with a low risk reported in another study [47]. One additional study [26•] conducted in Medicaid-enrolled youths, detected higher risk for diabetes incident for SGA initiators concomitantly to antidepressant use (odds ratio [OR] 1.54, 95% CI 1.17–2.03, p = 0.002), when compared to only SGA initiators. Furthermore, first-episode and antipsychotic-naïve patients with schizophrenia as compared to chronic patients are more vulnerable to severe weight gain, rapidly during the first few weeks, due to antipsychotics [47].

Antidepressants

The prevalence of depression in T2D is estimated 10–30% [48] and the comorbidity is associated with poor glycemic control, apart from increased T2D complications [49]. Literature results suggest that antidepressants could potentially influence T2D regulation, beneficial or deleteriously. Therefore, a review and meta-analysis of 14 randomized control trials [50] suggests sertraline (Selective Serotonin Reuptake Inhibitors, SSRIs) for better glycemic control, as no effect was detected by nortriptyline (Tricyclic Antidepressant, TCAs), paroxetine (SSRIs), and fluoxetine (SSRIs).

On the other hand, there is a considerable literature on the potential diabetogenic adverse effects of antidepressants, partially through inducing weight gain [51], mainly after exposure to high Histamine1-receptor (H1) affinity ADs [52]. Similarly, hyperglycemia was linked to the use of high affinity H1 and 5-hydroxy-tryptamine 2c [5HT2c] receptors in a study conducted with the Adverse Drug Reaction Database [53]. Sedative effect, the increase in appetite, and weight gain induced by ADs represent the most popular factors linking ADs with T2D [54,55,56]. A review of 17 case reports [57, 58] detected hyperglycemia between 3 weeks and 5 months after antidepressant treatment initiation of paroxetine, clomipramine and mirtazapine, a reversible effect within a week after drug abstinence. Cross-sectional studies, such as the Finish Prevalence, Prediction and Prevention of Diabetes (FFD) program [59, 60] and the Hordaland Health Survey, Norway, comparing 461 patients taking SSRIs with 25,315 not taking [61] detected no association between antidepressant use and T2D.

On the other hand, the population-based cross-sectional National Health and Nutrition Examination Studies [62] exploring the association between pre-diabetes and T2D with depression and antidepressant use identified significant linkage, when antidepressants were applied (OR 1.75 [95% CI 1.20–2.54]). Further, case-control studies provide evidence of diabetogenic effect of antidepressants. Specifically, the U.K. General Practice Research Database [63], including a cohort of 165,958 patients with depression, detected increased risk of T2D (OR 1.84 CI [1.35–2.52]) by moderate to highly daily dose of antidepressants use for over 24 months, for both SSRIs and TCAs. Similarly, a Finnish occupational study comparing 851 people who developed T2D with 4234 T2D free people [64], evaluated increased risk of T2D in individuals consuming ADs with severe depression (OR 2.65 [CI 1.31–5.39]) or even without (OR 1.93 [CI 1.48–2.51]).

Furthermore, a Canadian case-control study [65], aiming to evaluate the magnitude of the diabetogenic effect of different antidepressant categories, detected no difference between TCAs and SSRIs (OR 1.05[CI 0.86–1.28], whereas the diabetogenic effect was significantly elevated when SSRIs and TCAs were applied concurrently, as compared with TCAs alone (OR 1.89 [CI 1.35–2.65]). Another retrospective cohort study [66], comparing 31,552 adults under antidepressant treatment and 9136 under benzodiazepine prescription from Texas Medicaid database, evaluated double elevated T2D risk with antidepressants, while the association was estimated also separately for the TCAs (HR 1.759 [95% CI 1.517–2.040]), for serotonin-norepinephrine reuptake inhibitors (SNRIs) (HR 1.566 [95% CI 1.351–1.816]), SSRIs (HR 1.481 [95% CI 1.318–1.665]) and other antidepressants (HR 1.376 [95% CI 1.198–1.581]). On the contrary, the Dutch pharmacy database study [67] following 60,516 individuals from initiation of antidepressants, benzodiazepine, and diabetes treatment, estimated almost no risk for T2D onset under antidepressants (HR 1.05 [95% CI 0.88–1.26]), higher for benzodiazepine use (HR 1.37 [95% CI 1.12–1.68]), and even higher (HR 1.37 [95% CI 1.12–1.68]) for the concomitant use of both ADs and benzodiazepines.

A study evaluated elevated risk of T2D in patients with moderate to severe depression by 93–165% compared with the general population, when applied conventional antidepressants [64, 68, 69], though not in a causal way. Further, treatment short-termly with SSRIs, the most frequently prescribed antidepressants, improves glucose regulation in the general population [70], whereas no glycaemic dysregulation was detected after 1 year use of SSRIs in patients with established T2D [71], potentially due to its known anorexigenic properties [72]. A placebo-controlled trial of an antidepressant [73], as well as an observational study [74] comparing glycaemic traits before and after antidepressant therapy in people with depression failed to detect effects on insulin sensitivity, despite the improvement in depression management. Further, two other studies present improved insulin resistance in patients with depression under AD therapy [75, 76]. On the contrary, long-term application of at least moderate doses of antidepressants (TCAs and SSRIs) has been linked with elevated T2D risk [64, 77, 78]. A meta-analysis, though involving only observational studies, detected elevation in diabetes onset likelihood (OR 51.50 [95% CI 1.08–2.10], HR 51.19, [95% CI: 1.08–1.32]) [79]. Finally, most studies [47, 80] provide evidence for increased diabetes risk with the concurrent use of TCAs and SSRIs (OR = 1.89) [65], the long-term use of both tricyclic TCAs (incidence rate ratio, IRR = 1.77) and SSRIs (IRR = 2.06) when applied in at least moderate daily doses [77], as well as when use of antidepressant medication refers to highly-risk patients [81]. Further, amitriptyline, imipramide, and mirtazapine are associated substantially with weight gain, nortriptyline and paroxetine seem to have intermediate effect, whereas bupropion and fluoxetine are related to weight loss [22] (Table 2).

Table 2 Review of antidepressants and mood stabilizers effects on diabetogenic risk and weight gain

Outcomes of all these studies should be interpreted with caution, due to heterogeneity of methodological structure making often comparisons between studies impossible or on ground of differences in the population examined, whether they refer to the general population or specifically to samples with depression, who more often undertake diabetes screening [63, 86, 87]. Furthermore, conflicting results could be ascribed to disparities in each antidepressant drug molecule or group effect, or consequence of different glycemic traits measured between different studies, such as insulin secretion, insulin resistance [75, 88, 89]. Finally, high rates of off-label psychotropic medication application strengthen the request for clinical trials to better estimate the efficacy and safety of these treatments [77].

Other Psychotropic Medications

Little research has been held to evaluate the potential diabetogenic effect of other psychiatric regiments applied to manage SMI, or in terms of their synergistic action, when they are applied concomitantly with antipsychotics or ADs. Mood stabilizers, especially valproate [82] and lithium [83] (Table 2), have been associated with insulin resistance and diabetes risk,[84, 90] related possibly to weight gain [91], and/or fatty liver infiltration [92]. Other studies also relate valproate with increased levels of triglycerides and glucose, and insulin abnormalities [85].

Conversely, in youth with concomitant ADs and stimulant use, the duration of stimulant use or the cumulative stimulant doses were not associated with T2D onset [26•, 93•]. Further, the concomitant with ADs application of anxiolytics, alpha 2 adrenergic agonists and hypnotics in the youths revealed no additional T2D risk [26•]. Another study detected no effect of anxiolytics, and/or hypnotics use on HbA1c levels [94].

Prevention and Therapy

Clinical practice guidelines and individualized medicine are keys to improve health of patients with SMI. Overall, literature suggests SSRIs as safer choice in terms of T2D prevention. Concerning tricyclic antidepressants studies present a tendency towards increasing T2D risk, although causality is not established, therefore closer glucose monitoring is recommended when applied. Furthermore, among second generation agents, olanzapine and clozapine seem to have the strongest diabetogenic potential, however almost all antipsychotics (FGA, SGA) are associated with diabetogenic effects, noticeably at younger age, due to low background risk for T2D [95]. Additionally, mood stabilizers seem to elevate T2D risk.

The American Diabetes Association (ADA) highlights the importance of patients’ annual screening for people with SMI for pre-diabetes or diabetes. To test for T2D diabetes, fasting plasma glucose, 2-h plasma glucose after 75-g oral glucose tolerance test, and HbA1c are equally appropriate. Changes in weight, glycemic control, blood pressure, and cholesterol levels should be carefully monitored and the treatment regimen should be reassessed [96]. Foremost, motivation in the direction of healthy lifestyle choices, such as tobacco cessation, weight management, healthy eating, sleep quality, physical activity, and effective strategies for coping with stress represent priorities for health providers. Notwithstanding these, collaborative, multidisciplinary teams are best suited to provide care for people with chronic conditions such as SMI and to facilitate patients’ self-management. Prioritizing timely and appropriate intensification of lifestyle and/or pharmacological therapy for patients who have not achieved the recommended metabolic targets, redefining the roles of the health care delivery team and empowering patient self-management are fundamental to achieve diabetes prevention and bring optimal therapeutic results [96]. HbA1c control every three 3 months, fasting lipid profile, including total, LDL (low density cholesterol), and HDL cholesterol (high-density cholesterol) and triglycerides, liver function tests, spot urinary albumin–to–creatinine ratio, serum creatinine and estimated glomerular filtration rate belong to the regular monitoring plan of T2D patients. Vaccination against pneumonia for all people with T2D through 64 years of age, additionally to vaccination against influenza for all T2D patients is highly recommended. Particular attention should be paid in the follow up of SMI people, under regular treatment with combinations of antipsychotic, antidepressants and MS, given the limited data on the diabetogenic adverse effects of combination regimes.

Conclusion

This review implies the association between specific antidepressants, such as tricyclics and antipsychotics, applied separately or concomitantly with the incidence of T2D. On the contrary, other ADs, such as SSRIs, are considered to be neutral, or even beneficial over the short-term use, leading to a better control of depressive symptoms and encouraging actions in the direction of a more advantageous T2D self-management. Given the high prevalence of AD and antipsychotic use and the heterogeneity inside each medication category, a finer classification according to their pharmacological profile, could serve in better elucidating the nature and magnitude of this association. Comprehensive evaluation of the risk of T2D associated to psychiatric medication is becoming of utmost importance for the clinicians to help patients follow efficient and safe treatments. Future large sample, longitudinal, highly phenotyped studies could help drawing definite recommendations on medications safety.