See KC. Impact of inhaled and intranasal corticosteroids on glucose metabolism and diabetes mellitus: A mini review. World J Diabetes 2023; 14(8): 1202-1211 [PMID: 37664474 DOI: 10.4239/wjd.v14.i8.1202]
Corresponding Author of This Article
Kay Choong See, FCCP, FRCP, MBBS, MRCP, Adjunct Associate Professor, Department of Medicine, National University Hospital, 1E Kent Ridge Road, Level 10 NUHS Tower Block, Singapore 119228, Singapore. mdcskc@nus.edu.sg
Research Domain of This Article
Respiratory System
Article-Type of This Article
Minireviews
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Author contributions: See KC collected the data, wrote the paper, read and approved the final manuscript.
Conflict-of-interest statement: The author reports no relevant conflicts of interest for this article.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Kay Choong See, FCCP, FRCP, MBBS, MRCP, Adjunct Associate Professor, Department of Medicine, National University Hospital, 1E Kent Ridge Road, Level 10 NUHS Tower Block, Singapore 119228, Singapore. mdcskc@nus.edu.sg
Received: February 11, 2023 Peer-review started: February 11, 2023 First decision: May 15, 2023 Revised: May 28, 2023 Accepted: July 11, 2023 Article in press: July 11, 2023 Published online: August 15, 2023 Processing time: 180 Days and 23.7 Hours
Abstract
Inhaled corticosteroids (ICS) and intranasal corticosteroids (INS) are the mainstays of treatment for chronic respiratory diseases like asthma, chronic obstructive pulmonary disease, and allergic rhinosinusitis. In addition, these localized forms of steroid therapy are generally considered to have fewer systemic side effects compared to long-term oral corticosteroids. However, concern and controversy remain over the impact of ICS and INS on the incidence and control of diabetes mellitus (DM). Given the widespread use of ICS and INS, even small individual effects on DM could lead to large consequences for the global popu-lation. Multiple large observational studies suggest that high dose ICS is associated with increased incident DM and worsened DM control, though the contribution of other risk factors is less certain. In addition, only two studies were done to investigate the association of INS and DM, with both studies demon-strating a short-term association of INS use with hyperglycemia. While more research evaluating the risk of ICS/INS for DM-related adverse events is needed, high doses of ICS/INS should be avoided when possible. The following strategies for ICS/INS dose minimization can be considered: Use of non-pharmacological measures (trigger avoidance, smoking cessation, vaccination to avoid infection), control of comorbid conditions, use of non-ICS-containing medications, inter-mittent rather than regular ICS dosing, and appropriate de-escalation of high ICS doses.
Core Tip: Inhaled corticosteroids (ICS) and intranasal corticosteroids (INS) are the mainstays of treatment for chronic respiratory diseases like asthma, chronic obstructive pulmonary disease, and allergic rhinosinusitis. Multiple large observational studies suggest that high dose ICS is associated with increased incident diabetes mellitus (DM) and worsened DM control, though the contribution of other risk factors is less certain. In addition, only two studies were done to investigate the association of INS and DM, with both studies demonstrating a short-term association of INS use with hyperglycemia.
Citation: See KC. Impact of inhaled and intranasal corticosteroids on glucose metabolism and diabetes mellitus: A mini review. World J Diabetes 2023; 14(8): 1202-1211
Corticosteroids are important anti-inflammatory drugs that are widely used in respiratory disease. Inhaled corticosteroids (ICS) are the mainstay of treatment for patients with asthma[1]. ICS are also added to dual bronchodilators for patients with chronic obstructive pulmonary disease (COPD) who have frequent exacerbations and peripheral eosinophilia ≥ 300 cells/μL[2]. Like ICS for asthma and eosinophilic COPD, intranasal corticosteroids (INS) are the key medi-cations to treat allergic rhinitis[3]. Given the high global prevalence of asthma, COPD, and allergic rhinitis, widespread use of ICS and INS is expected[4,5].
Diabetes mellitus (DM) is another disease with a high global burden[6]. Complications of uncontrolled DM include coronary artery disease, peripheral vascular disease, kidney failure, and eye disease, and can be a serious threat to both quality of life and survival[7]. As such, reducing both the development of DM, and the worsening of DM control, would be crucial in reducing the global burden of DM. Apart from antidiabetic drugs, prevention of chronic hyperglycemia would also be helpful. Therefore, long-term use of drugs that impair glucose metabolism, such as oral steroids, should be avoided[8]. However, it is uncertain if ICS and INS have systemic effects on glucose metabolism, and if ICS and INS increase the risk of incident DM (i.e., development of new cases of DM) or worsen DM control. Therefore, this paper will use clinical data from human studies and review the impact of ICS and INS on DM incidence or control.
PHARMACOLOGY OF ICS AND INS
Corticosteroids are synthetic glucocorticoids, which differ in glucocorticoid receptor binding affinity and potency[9]. For ICS and INS, all corticosteroids are administered as active forms, except for beclomethasone dipropionate and ciclesonide, which are prodrugs requiring metabolism to active forms. The more potent agents used as ICS and INS are fluticasone furoate, mometasone furoate, fluticasone propionate, beclomethasone dipropionate (via its active metabolite beclomethasone monopropionate), and ciclesonide (via its active metabolite desisobutyryl ciclesonide). The less potent agents used as ICS and INS are budesonide, triamcinolone acetonide, and flunisolide. In general, the more potent glucocorticoids can be used in smaller doses to achieve the same anti-inflammatory effect as the less potent agents. In addition, given lower delivered doses, use of more potent glucocorticoids does not necessarily translate into more adverse effects.
For ICS, the delivered dose enters the systemic circulation via two routes[10]. The first route is via the gastrointestinal tract, where 60%-90% of the delivered dose is deposited in the oropharynx, swallowed into the stomach, absorbed through the intestines, and metabolized by the liver. Hepatic metabolism renders most of the systemically absorbed ICS inactive, even for corticosteroids with significant oral bioavailability (e.g., beclomethasone dipropionate, budesonide, triamcinolone acetonide, and flunisolide). The second route by which ICS enters the systemic circulation is via the lungs, where the remaining 10%-40% of the delivered dose passes directly into the systemic circulation. ICS absorbed via the lung bypasses hepatic first-pass metabolism, and exerts greater systemic impact compared to ICS absorbed via the gastrointestinal tract.
For INS, the drug is sprayed as an aqueous suspension into the nose, with a relatively short dwell time of < 1 h[3]. Given rapid nasal ciliary clearance, much of the drug runs off after some absorption into the nasal mucosa. As such, systemic effects, if any, would arise from entry via the gastrointestinal tract. Like swallowed ICS, swallowed INS would also undergo first-pass metabolism in the liver with oral bioavailability depending on the type of corticosteroid.
EFFECT OF ICS AND INS ON GLUCOSE METABOLISM AND DM
Glucocorticoids drive hyperglycemia via increased hepatic gluconeogenesis and decreased hepatic/adipocyte glucose uptake, mediated by the glucocorticoid receptor in the cytoplasm of peripheral tissues (primarily liver, skeletal muscle, and adipose tissue)[11-13] (Figure 1) and possibly by hepatic activation of Krüppel-like factor 9[14]. Risk factors for hyperglycemia involve patient factors and drug factors. Patient factors include age and diseases that predispose to hyperglycemia such as obesity. Drug factors include ICS/INS dose, corticosteroid formulation/potency, regular vs intermittent use of ICS/INS, and medications that inhibit cytochrome P450 3A4 and therefore hepatic metabolism of systemically absorbed ICS/INS. When hyperglycemia becomes chronic, DM and its complications may develop. Biochemically, chronic hyperglycemia can be reflected as elevations of fructosamine (indicates average serum glucose concentration over the preceding 2-3 wk)[15] and, more commonly, glycated hemoglobin (HbA1c).
Figure 1 Molecular signaling pathway of glucocorticoid-induced hyperglycaemia.
GC: Glucocorticoid; G6Pase: Glucose-6-phosphatase, encoded by G6PC1; HSD1: Hydroxysteroid dehydrogenase type 1; IRS: Insulin receptor substrate; NEFA: Non-esterified fatty acid; PEPCK: Phosphoenolpyruvate carboxykinase, encoded by PCK1; PI3K: Phosphatidylinositol 3-kinase; PKB-AKT: Protein kinase B; PPAR: Peroxisome proliferator-activated receptor. Open-source clipart images from freesvg.org and scidraw.io.
Clinical studies investigating the association of ICS/INS have differing results. Some show no worsening of glucose metabolism or DM (Table 1), while others show worsening (Table 2). Multiple study designs from case reports to randomized control trials have been employed, with the largest studies tapping on population registries. All the studies explored ICS as the exposure variable, while only two studies focused on INS[16,17].
Table 1 Studies showing no worsening of glucose metabolism/diabetes mellitus by inhaled corticosteroid/intranasal corticosteroid.
Off-label use of otic ciprofloxacin 0.3%/dexamethasone 0.1% drops in the nasal passage for choanal obstruction with granulation tissue
Over 7 d, average daily blood glucose increased by 86 mg/dL. Hyper-glycemic spikes resolved within 2 d after switching to mometasone furoate 0.05% spray
Over 4 wk, ICS use associated with increased peak blood glucose (7.1 versus 6.7 mmol/L, P < 0.01) after 75 g oral glucose load. No effect on fasting blood glucose or HbA1c
Children who were born January 1, 1995, through December 31, 2008, in Finland and diagnosed with type 1 DM by 2010 (n = 3342), compared with 10% random sample from each birth-year cohort (n = 80909)
Beclomethasone, BUD, fluticasone. Dose not stated
Over a median of 7.9 yr, increased risk of type 1 DM after adjusting for other anti-asthmatic drugs, asthma, sex, and birth decade (HR = 1.29, 95%CI: 1.09-1.52), if patients received high-dose ICS (> 800 mcg budesonide equivalent dose)
1768 DM patients treated with INS, with 245 patients providing HbA1c data and 163 patients providing fasting glucose data
BUD, FP, triamcinolone acetonide INS. Dose not stated
Over 3 mo, triamcinolone acetonide associated with increased fasting glucose but not with HbA1c. Other INS had no association with either glucose or HbA1c changes
682 adults (≥ 40 years old) with COPD prescribed ICS in two large United Kingdom databases (1983-2016)
Types and doses of ICS not stated
Over 12-18 mo of follow-up, ICS prescription associated with increased HbA1c, with adjusted difference 0.16% (95%CI: 0.05%-0.27%) in all COPD patients, and 0.25% (95%CI: 0.10%-0.40%) in mild-to-moderate COPD patients. ICS prescription also associated with more diabetes-related general practice visits and more frequent glucose strip prescriptions. Associations were stronger for higher cumulative ICS doses (> 250 mg FP equivalent), compared to ≤ 125 mg
18774 adults (≥ 40 years old) with COPD initiating ICS or long-acting bronchodilator in two large United Kingdom databases (1983-2016)
Types and doses of ICS not stated
Over a median follow-up at least 3.5 yr, ICS use associated with increased risk of incident DM (HR = 1.27, 95%CI: 1.07-1.50). ICS use also worsened DM control for high-dose ICS (mean daily dose ≥ 500 mcg FP equivalent)
Predominantly BUD (about 50%) and fluticasone (about 45%) ICS, at various doses. Other ICS (< 5%) used included beclomethasone, ciclesonide and mometasone
Over 7 yr, ICS use was associated with an increased risk of DM (HR = 1.16, 95%CI: 1.01-1.32) for high-dose ICS use (≥ 970 mcg BUD equivalent) and BMI < 30 kg/m2
1698 adults with COPD, among United States veterans enrolled in 7 primary care clinics between February 1997 and December 1999
Various types (e.g., beclomethasone, flunisolide, fluticasone) and doses of ICS
Over 2-4 yr, among diabetics only, there was a 1.82 mg/dL (95%CI: 0.49-3.15) increase in serum glucose, for every 100-mcg triamcinolone equivalent/d increase in ICS dose
Nested case-controlled study using a Canadian health insurance database
388584 patients with respiratory disease
Various types of ICS (beclomethasone, BUD, triamcinolone, fluticasone, flunisolide), at various doses
Over 5.5 yr of follow-up, 34% increased rate of initiation of an anti-diabetic agent, especially in patients receiving high dose ICS (≥ 1000 mcg/d FP equivalent). In diabetics on oral hypoglycemic agents, ICS use increased risk of progression to insulin
Among the studies showing no worsening of glucose metabolism/DM by ICS/INS (Table 1), patients with both asthma and COPD were followed up for as long as three years[18,19]. The doses of ICS/INS range from intermediate to relatively high doses (up to 2000 mcg/d of beclomethasone dipropionate ICS, and up to 1600 mcg/d of budesonide ICS)[20]. Some studies, though large, did not collect DM-related adverse events purposefully, which can lead to false negative findings (i.e., finding no association when a real association is present). For instance, in a pooled analysis of 68 randomized trials for ICS (60 for asthma; 8 for COPD), the number of DM-related adverse events relied on spontaneous adverse event reports only, without formal biochemical validation of DM[21].
Among the studies showing worsening of glucose metabolism/DM by ICS/INS, the smaller studies generally use relatively high doses of ICS (up to budesonide ICS 2000 mcg daily and fluticasone propionate ICS 2000 mcg/d) and demonstrated laboratory abnormalities related to hyperglycemia (e.g., increased HbA1c, glycosuria). Both studies involving INS demonstrated hyperglycemia[16,17]. The case report involving INS suggests that dose matters, as off-label use of high-dose INS in an infant with type 1 DM resulted in hyperglycemia, which resolved when the INS was switched to a standard low-dose formulation[17].
Nonetheless, laboratory abnormalities do not necessarily translate into DM. Development of new DM has only been uncovered in large observational studies[22-27]. Within these large datasets, the risk factors for incident DM associated with ICS/INS use are not always obvious, though some studies have ascribed increased DM risk with higher ICS doses[25-29]. For example, using a Canadian health insurance database, Suissa et al[27] studied 388584 patients with respiratory disease, and found that current use of ICSs had a 34% increase in the incidence rate of DM [rate ratio (RR) = 1.34; 95% confidence interval (CI): 1.29-1.39] and a similar increase in the incidence rate of worsening DM control (RR = 1.34, 95%CI: 1.17-1.53). The RRs were greatest for the highest ICS doses, equivalent to at least 1000 mcg/d fluticasone: RR for incident DM 1.64, 95%CI: 1.52-1.76; RR for worsening DM control 1.54, 95%CI: 1.18-2.02. However, apart from ICS dose, and the possible role of increased bioavailability of triamcinolone INS contributing to hyperglycemia[16], other patient-specific or corticosteroid-specific risk factors have not been well-studied.
REDUCING THE IMPACT OF ICS AND INS ON GLUCOSE METABOLISM AND DM
From existing studies, the impact of ICS/INS on glucose metabolism and DM is inconsistent, though the reasons for inconsistency are not completely apparent. Nevertheless, ICS dose has been repeatedly identified as a risk factor in large observational studies, which would have adequate power to uncover significant associations between dose and incident DM. In addition, in the only 2 studies focused on INS, high INS doses were associated with hyperglycemia. Therefore, it is prudent that ICS/INS doses are minimized to obtain benefit while avoiding potential hyperglycemia and DM.
Strategies to minimize ICS and INS doses are outlined in Table 3. In general, non-pharmacological measures should be used to optimize disease control and reduce the reliance on high dose ICS/INS formulations. These non-pharmacological measures include trigger avoidance, smoking cessation, and vaccination to avoid infection. Holistic management of environmental triggers and comorbid conditions such as obesity, obstructive sleep apnea, cardiac dysfunction, anxiety, and depression can be considered as part of a “treatable traits” approach to improve the care of patients with chronic respiratory disease, further reducing the need for high dose ICS/INS. Using this approach, physiological, biochemical, psychosocial, microbiological, and comorbidity traits are targeted with both pharmacological and non-pharmacological interventions[30].
Table 3 Methods to reduce the impact of inhaled corticosteroid and intranasal corticosteroid on glucose metabolism and diabetes mellitus.
Strategy
Methods
Minimize ICS doses
Use non-pharmacological measures (e.g., trigger avoidance, smoking cessation, vaccination to avoid respiratory infections) to optimize disease control and reduce the need for high dose ICS[2]
Manage comorbid conditions to optimize disease control (e.g., management of obesity, OSA, heart failure, anxiety, depression) and reduce the need for high dose ICS. Consider using the “treatable traits” approach for holistic management of chronic respiratory diseases[30]
Use long-acting bronchodilators to reduce the need for high dose ICS[2]
Ensure good inhaler technique (or use valved holding chamber) to improve lung delivery and effectiveness of ICS, reducing the need for high dose ICS[2]
Consider intermittent formoterol-ICS therapy rather than regular ICS for asthma[31]
Actively step-down regular ICS dosing, including changing regular to intermittent ICS use, by clinical assessment[31]
Actively step-down regular ICS dosing by measuring FENO in asthma[32]
Actively step-down or step-off ICS if peripheral eosinophil count < 300/μL in well-controlled COPD[2]
Minimize INS doses
Use non-pharmacological measures (e.g., trigger avoidance, smoking cessation, vaccination to avoid respiratory infections) to optimize disease control and reduce the need for high dose INS[56]
Use non-steroidal medications like intranasal antihistamines to reduce the need for high dose INS[56]
Ensure good intranasal delivery technique to improve effectiveness of INS, reducing the need for high dose INS
Actively step-down regular INS dosing, including changing regular to intermittent INS use, following clinical assessment, e.g., as-needed intranasal corticosteroids for seasonal allergic rhinitis[57]
Maintain hepatic inactivation of ICS and INS
Avoid strong CYP450 3A4 inhibitors like clarithromycin, itraconazole, ketoconazole, and voriconazole[3,9]
Weight management for overweight and obese patients[58]
Ensure good glycemic control for diabetic patients[58]
Additionally, non-ICS-containing medications may also be used to improve disease control, e.g., use of long-acting bronchodilators in asthma and COPD[2]. If ICS/INS are needed, dosing strategies such as intermittent dosing can be employed. For asthma, compared to regular ICS use, intermittent dosing with ICS-formoterol has proven to be as effective for prevention of exacerbations in patients with mild asthma, with reduced cumulative exposure to ICS[31]. Finally, de-escalation of high ICS/INS doses should be considered when following up patients with well-controlled disease. Apart from clinically directed de-escalation, biomarkers such as blood eosinophil count can guide clinicians when reducing ICS exposure in COPD[2]. Similarly, exhaled nitric oxide may guide clinicians when reducing ICS exposure in asthma[32].
Although not supported by specific studies, given the pharmacology of ICS, avoidance of strong CYP450 3A4 inhibitors (e.g., clarithromycin, itraconazole, ketoconazole, voriconazole) can preserve the high first-pass metabolism and hepatic inactivation of swallowed ICS and INS. Furthermore, it will be prudent to avoid other causes of hyperglycemia and DM, such as regular, high-dose oral corticosteroids.
FUTURE DIRECTION
Some systemic absorption of ICS/INS is inevitable, and systemic effects would be proportional to the dose of delivered. Apart from dose, other potential risk factors require further elucidation. Nevertheless, even if risk factors have for susceptibility to ICS/INS-related DM are identified, it is unknown how patients who receive ICS or INS should be screened or monitored. Therefore, future studies need to address both risk factors for DM-related complications of ICS/INS as well as mitigation of DM-related risk. In addition, special populations such as pregnant women require more study[33].
Also, only two studies involving INS have been done to investigate its relationship with hyperglycemia[16,17]. Although the studies demonstrate an adverse association of INS with fasting glucose levels, a more chronic effect is not apparent given the lack of association with HbA1c level. More research for INS is therefore required. These studies need to be large enough to uncover small but significant associations, and long enough to identify chronic hyperglycemia leading to incident DM.
Efforts to disentangle the desired anti-inflammatory effects and diabetogenic consequences of glucocorticoids have led to the discovery of several candidate pharmacological compounds[11]. Selective glucocorticoid receptor agonists and selective glucocorticoid receptor modulators can preserve anti-inflammatory function and minimize induction of hyperglycemia. For instance, caesaldekarine is a promising plant-derived compound that has selective glucocorticoid receptor modulator-like properties[34]. Another approach is to enhance insulin signaling and mitigate hyperglycemia via 11β-hydroxysteroid dehydrogenase type 1 inhibition[35].
CONCLUSION
Overall, the association of ICS/INS with DM cannot be ignored, especially given multiple large observational studies demonstrating a positive association and dose-response. As ICS/INS are widely used, even a small individual effect of ICS/INS on DM would be clinically significant on a population basis. To avoid under-recognition of DM-related adverse events, these events should be deliberately collected and validated in future observational cohorts and randomized trials involving ICS/INS. Meanwhile, although ICS/INS are critical agents for control of chronic respiratory diseases, harm minimization should be undertaken by patients and high doses avoided whenever possible.
Footnotes
Provenance and peer review: Invited article; Externally peer reviewed.
P-Reviewer: Aslam M, India; Nagamine T, Japan; Sukocheva OA, Australia; Zeng Y, China; Islam MS, South Africa S-Editor: Wang JJ L-Editor: A P-Editor: Chen YX
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