COVID-19 pandemic impact on people with diabetes: results from a large representative sample of Italian older adults

1. IntroductionCOronaVIrus Disease 2019 (COVID-19) outbreak quickly became a pandemic [

W. Coronavirus, 2021. Dashboard| WHO Coronavirus (COVID-19) Dashboard With Vaccination Data, in, 2021.

]. Italy was the first COVID-19 epicentre in Europe, and Lombardy was the region with the highest number of cases, hospital admissions and deaths [Odone A. Delmonte D. Scognamiglio T. Signorelli C. COVID-19 deaths in Lombardy, Italy: data in context.]. On the 9th of March 2020, Italy was also the first Western country to impose a nationwide stay-at-home order to reduce viral spread and alleviate pressure on the healthcare system [Signorelli C. Scognamiglio T. Odone A. COVID-19 in Italy: impact of containment measures and prevalence estimates of infection in the general population.]. In compliance with these non-pharmaceutical interventions (NPIs) and those followed in the second half of 2020 (e.g., geographical restrictions, physical distancing, school and other services closures, hand hygiene and respiratory etiquette prescriptions) [Ayouni I. Maatoug J. Dhouib W. Zammit N. Fredj S.B. Ghammam R. Ghannem H. Effective public health measures to mitigate the spread of COVID-19: a systematic review.], radical changes occurred in Italians' daily life and behaviours, impacting social, working, and family habits, and access to daily-life services [Philpot L.M. Ramar P. Roellinger D.L. Barry B.A. Sharma P. Ebbert J.O. Changes in social relationships during an initial “stay-at-home” phase of the COVID-19 pandemic: a longitudinal survey study in the US.].This situation was responsible for exacerbating pre-existing health, socioeconomic, and geographic inequalities, with greater consequences among vulnerable populations [Bambra C. Riordan R. Ford J. Matthews F. The COVID-19 pandemic and health inequalities.], whose susceptibility is likely to worsen health outcomes.Among disadvantaged groups, individuals with a chronic disease, such as diabetes, and frail individuals, such as the elderly, were more exposed than other categories [Abdi A. Jalilian M. Sarbarzeh P.A. Vlaisavljevic Z. Diabetes and COVID-19: A systematic review on the current evidences.], and the two vulnerabilities generally add up [Wild S. Roglic G. Green A. Sicree R. King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030.]. Both lifestyles [Lambrinou E. Hansen T.B. Beulens J.W. Lifestyle factors, self-management and patient empowerment in diabetes care., Environmental/lifestyle factors in the pathogenesis and prevention of type 2 diabetes., Zheng Y. Ley S.H. Hu F.B. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications.] and healthcare services [Beran D. Aebischer Perone S. Castellsague Perolini M. Chappuis F. Chopard P. Haller D.M. Jacquerioz Bausch F. Maisonneuve H. Perone N. Gastaldi G. Beyond the virus: ensuring continuity of care for people with diabetes during COVID-19.] are critical to enhance the quality of patients’ life. Health behaviours, mental health, primary and hospital care use are interrelated determinants and potential risk factors for older people’s wellbeing, diabetes evolution and management.Available data on the impact of NPIs on health are inconsistent and inconclusive: cross-sectional assessments generally suggest an overall detrimental role of the pandemic and restrictions on lifestyles, mental health, and addictions [Catucci A. Scognamiglio U. Rossi L. Lifestyle changes related to eating habits, physical activity, and weight status during COVID-19 quarantine in Italy and some European Countries., Fiorillo A. Sampogna G. Giallonardo V. Del Vecchio V. Luciano M. Albert U. Carmassi C. Carrà G. Cirulli F. Dell'Osso B. Nanni M.G. Pompili M. Sani G. Tortorella A. Volpe U. Effects of the lockdown on the mental health of the general population during the COVID-19 pandemic in Italy: Results from the COMET collaborative network.]. Our previous studies on a representative sample of Italian households [Odone A. Lugo A. Amerio A. Borroni E. Bosetti C. Carreras G. Cavalieri d'Oro L. Colombo P. Fanucchi T. Ghislandi S. Gorini G. Iacoviello L. Pacifici R. Santucci C. Serafini G. Signorelli C. Stival C. Stuckler D. Tersalvi C.A. Gallus S. COVID-19 lockdown impact on lifestyle habits of Italian adults.] showed huge implications on mental health symptoms [Amerio A. Lugo A. Stival C. Fanucchi T. Gorini G. Pacifici R. Odone A. Serafini G. Gallus S. COVID-19 lockdown impact on mental health in a large representative sample of Italian adults.], smoking habits [Carreras G. Lugo A. Stival C. Amerio A. Odone A. Pacifici R. Gallus S. Gorini G. Impact of COVID-19 lockdown on smoking consumption in a large representative sample of Italian adults.], addictive behaviours [Lugo A. Stival C. Paroni L. Amerio A. Carreras G. Gorini G. Mastrobattista L. Minutillo A. Mortali C. Odone A. Pacifici R. Tinghino B. Gallus S. The impact of COVID-19 lockdown on gambling habit: a cross-sectional study from Italy.], and sexual activity [Amerio A. Lugo A. Bosetti C. Fanucchi T. Gorini G. Pacifici R. Odone A. Gallus S. Italians Do It … Less. COVID-19 lockdown impact on sexual activity: evidence from a large representative sample of Italian adults.].Thus far, there are no unequivocal results regarding the impact on people with diabetes, representing a specific vulnerable group in terms of attention paid to health behaviours, disease follow-up and compliance with treatments. Since hyperglicemia was the second most common comorbidity for COVID-19, after hypertension, and its management deeply relies on lifestyles and routine care [Farahani F. Mirzaei F. Khodadadi I. Abbasi-Oshaghi E. Importance of hyperglycemia in preoperative, intraoperative and postoperative periods in COVID-19 patients., Mirzaei F. Khodadadi I. Vafaei S.A. Abbasi-Oshaghi E. Tayebinia H. Farahani F. Importance of hyperglycemia in COVID-19 intensive-care patients: mechanism and treatment strategy.], assessing these aspects is crucial, especially with available evidence referring to non-representative hospital-recruited samples and forbidding results' generalisation [Sacre J.W. Holmes-Truscott E. Salim A. Anstey K.J. Drummond G.R. Huxley R.R. Magliano D.J. van Wijngaarden P. Zimmet P.Z. Speight J. Shaw J.E. Impact of the COVID-19 pandemic and lockdown restrictions on psychosocial and behavioural outcomes among Australian adults with type 2 diabetes: findings from the PREDICT cohort study., Hansel B. Potier L. Chalopin S. Larger E. Gautier J.F. Delestre F. Masdoua V. Visseaux B. Lucet J.C. Kerneis S. Abouleka Y. Thebaut J.F. Riveline J.P. Kadouch D. Roussel R. The COVID-19 lockdown as an opportunity to change lifestyle and body weight in people with overweight/obesity and diabetes: results from the national French COVIDIAB cohort., Tanji Y. Sawada S. Watanabe T. Mita T. Kobayashi Y. Murakami T. Metoki H. Akai H. Impact of COVID-19 pandemic on glycemic control among outpatients with type 2 diabetes in Japan: a hospital-based survey from a country without lockdown.].Within the ‘LOckdown and lifeSTyles in Lombardia’ (LOST in Lombardia) study [Wang Y. Lugo A. Amerio A. d'Oro L.C. Iacoviello L. Odone A. Zucchi A. Gallus S. Stuckler D. The impact of COVID-19 lockdown announcements on mental health: quasi-natural experiment in Lombardy, Italy., Bonaccio M. Gianfagna F. Stival C. Amerio A. Bosetti C. Cavalieri d'Oro L. Odone A. Stuckler D. Zucchi A. Gallus S. Iacoviello L. Changes in a Mediterranean lifestyle during the COVID-19 pandemic among elderly Italians: an analysis of gender and socioeconomic inequalities in the "LOST in Lombardia" study., Stival C. Lugo A. Bosetti C. Amerio A. Serafini G. Cavalieri d'Oro L. Odone A. Stuckler D. Iacoviello L. Bonaccio M. van den Brandt P.A. Zucchi A. Gallus S. COVID-19 confinement impact on weight gain and physical activity in the older adult population: data from the LOST in Lombardia study., Jarach C.M. Lugo A. Stival C. Bosetti C. Amerio A. Cavalieri d'Oro L. Iacoviello L. Odone A. Stuckler D. Zucchi A. van den Brandt P. Garavello W. Cederroth C.R. Schlee W. Gallus S. The impact of COVID-19 confinement on tinnitus and hearing loss in older adults: data from the LOST in Lombardia study.], we investigated COVID-19 impact on physical and mental health outcomes, behavioural risk factors and access to care among older people with diabetes, in comparison with older people not affected by any chronic disease.2. Materials and methods2.1 Study design, setting and study population

LOST in Lombardia is a telephone-based cross-sectional study conducted in collaboration with Doxa, the Italian branch of the Worldwide Independent Network/Gallup International Association. Survey participants were selected among the Doxa panel and randomly recruited from a list of approximately 30,000 households living in the Lombardy region, representative by province and municipality size. A quota method was used to enrol study participants to guarantee the sample's representativeness, using quotas for sex, age group, and municipality size. A total of 4400 adults aged 65 years or more was recruited from the 17th of November to the 30th of November 2020.

The study protocol obtained approval from the ethics committee of Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy (file number 76, October 2020), and consent to participate was collected for all participants.

2.2 Questionnaire and variables of interest

Recruited subjects were interviewed using a telephone-based questionnaire about their lifestyles, health behaviours, mental distress, dietary habits, and access to healthcare services before and during the pandemic. The questionnaire included socioeconomic variables (age, sex, marital status, number of household members, educational level, employment, and self-reported economic status) and anthropometric data (height and weight before and after the pandemic). Subjects were asked whether they suffered from any common chronic disease (including diabetes, hypertension, other cardiovascular diseases, cancer, osteoarthritis or arthritis, osteoporosis, chronic kidney disease, asthma, chronic bronchitis or emphysema), about the year of each diagnosis and diseases' evolution during the pandemic.

Concerning health behaviours, participants were asked about physical activity (hours/week), smoking (cigarettes/day) and alcohol consumption (drinks/week) at the time of the interview (November 2020) and one year before (November 2019). They were also asked about their smoking status and years from smoking cessation. A specific section was dedicated to nutrition and dietary habits, asking participants about the changes in 8 food items consumption (unchanged, reduced, or increased with reference to November 2019), including those typical of the Mediterranean diet (i.e., fruit and nuts, vegetables, legumes, cereals, fish, milk and dairy products, meat and olive oil) to monitor eating habits patterns.

Regarding mental distress, we evaluated sleep quality and quantity, depressive and anxiety symptoms, through validated scales, with reference to both before and during the pandemic. Sleep quality and quantity were assessed using the Pittsburgh Sleep Quality Index (PSQI) questionnaire [Buysse D.J. Reynolds 3rd, C.F. Monk T.H. Berman S.R. Kupfer D.J. The pittsburgh sleep quality index: a new instrument for psychiatric practice and research.]. For the sleep quality evaluation, PSQI item number 9 was used. Participants were asked to answer also to PSQI item number 4, estimating how many hours of sleep they get at night. The presence of depressive symptoms was established using the 2-item Patient Health Questionnaire (PHQ-2), based on the 9-item validated scale (PHQ-9) [Kroenke K. Spitzer R.L. Williams J.B. The patient health questionnaire-2: validity of a two-item depression screener.]. Anxiety symptoms were assessed using the 2-item Generalised Anxiety Disorder (GAD-2), a short version of the 7-item scale (GAD-7) [Sapra A. Bhandari P. Sharma S. Chanpura T. Lopp L. Using generalized anxiety disorder-2 (GAD-2) and GAD-7 in a primary care setting.]. Higher PHQ-2 and GAD-2 scores during the pandemic than in 2019 stated worsening depressive and anxiety symptoms, respectively.

Changes in access to care were investigated asking participants about primary and hospital care, examinations and diagnostic tests, medicine purchase, using categorical answers (i.e., unchanged, reduced, or increased), while care delays (visits, surgeries, or therapies) were assessed with binary questions (yes, no). Details on the questionnaire’s items and categorisation used are provided in Appendix A.

Our exposure of interest was having diabetes vs not having any chronic disease. We considered as outcomes the changes in body mass index (BMI), physical activity, smoking habit, alcohol consumption and psychological measures, computed as the difference between the variables measured at the time of interview and a year before and categorised as unchanged, decreased or increased. Categorical variables about food consumption and healthcare services access were also investigated as outcomes.

2.3 Statistical analysis

We carried out the statistical analyses on a subgroup of 1826 older adults, of whom 947 (51.9 %) people with diabetes and 879 (48.1 %) subjects without any chronic condition. Descriptive analyses were reported as proportions or mean with standard deviation (SD), according to the exposure status. Group comparisons were performed using the chi-square test for categorical variables and t-test for the continuous ones.

We estimated odds ratios (ORs) and corresponding 95 % CIs for each outcome, using multinomial multivariable logistic regression models including diabetes vs no chronic diseases as independent variable. The models included educational level, marital and self-reported economic status as confounders on the basis of the existing literature. Moreover, a statistical weight has been used in the model to ensure the representativeness of the sample of Lombard older adults for age, sex, and municipality size.

Statistical analyses were carried out using Stata software version 16.0 (Stata Corporation, College Station, Texas, USA).

3. ResultsTable 1 reports the baseline distribution of sociodemographic characteristics and outcomes of interest according to the exposure status. People with diabetes compared to healthy ones were older (mean age 76.1 years vs 72.2 years), had fewer household members and more lived alone, had lower educational and socioeconomic status, and included more retired subjects. Exposed subjects were more overweight and obese, less current smokers who smoked few cigarettes/day, more alcohol consumers who drank more drinks/week, did less physical activity. Concerning psychological wellbeing, people with diabetes slept few hours/night, reported a poorer sleep quality, more anxiety and depressive symptoms.

Table 1Baseline distribution of 947 exposed subjects (with diabetes) and 879 unexposed ones (no chronic conditions) according to selected characteristics and outcomes.

Results from adjusted and weighted logistic regression models are reported in Table 2 for the behavioural and psychological outcomes, Table 3 for the dietary habits and Table 4 for access to healthcare services.

Table 2Odds ratios (ORs) and corresponding 95 % confidence intervals (CIs) from multinomial multivariable logistic regression models for the association between exposure and health behavioural and psychological outcomes.

Table 3Odds ratios (ORs) and corresponding 95 % confidence intervals (CIs) from multinomial multivariable logistic regression models for the association between exposure and dietary outcomes.

Table 4Odds ratios (ORs) and corresponding 95 % confidence intervals (CIs) from multinomial multivariable logistic regression models for the association between exposure and healthcare services access outcomes.

People with diabetes reported more frequently both a BMI increase (OR 1.69, 95 % CI 1.19–2.40) and decrease (OR 1.40, 95 % CI 1.05–1.86) than healthy subjects. Having diabetes was positively associated with an increased physical activity (OR 2.65, 95 % CI 1.69–4.13) and inversely associated with a reduced physical activity (OR 0.75, 95 % CI 0.60–0.94). People with diabetes also reported an OR of 6.27 (95 % CI 3.59–10.95) for drinks/week reduction compared to healthy individuals. No significant associations emerged neither for changes in smoking habits nor for sleep quantity, GAD-2 and PHQ-2 scores.

People with diabetes reported significant increases in the consumption of fruit and nuts (OR 2.06, 95 % CI 1.62–2.63), vegetables (OR 1.41, 95 % CI 1.10–1.82), fish (OR 2.51, 95 % CI 1.74–3.64) and olive oil (OR 3.54, 95 % CI 2.30–5.46), while decreases in the consumption of legumes and cereals intake (OR 2.21, 95 % CI 1.18–4.14 and OR 1.72, 95 % CI 1.01–2.91, respectively). No significant associations emerged for meat and meat products intake.

People with diabetes experienced more an increase of telephone contacts with GP (OR 3.70, 95 % CI 2.83–4.83), hospitalisations (OR 9.01, 95 % CI 3.96–20.51), diagnostic tests (OR 4.15, 95 % CI 2.62–6.56), self-pay specialistic visits (OR 2.93, 95 % CI 2.03–4.24) and medicine purchases with (OR 4.00, 95 % CI 2.52–6.35) and without a medical prescription (OR 2.37, 95 % CI 1.68–3.33). Having diabetes was positively associated with scheduled visits or surgeries cancelled or postponed both by the provider's (OR 2.47, 95 % CI 1.96–3.12) and patient's decision (OR 3.37, 95 % CI 2.58–4.42) and ongoing treatments interruption (OR 1.95, 95 % CI 1.33–2.86).

4. DiscussionFindings from our large representative sample of older adults support our hypothesis that COVID-19 lockdown and pandemic impacted differentially wellbeing of older people with diabetes compared to healthy older people. People with diabetes reported more frequently an improvement of selected lifestyles than healthy individuals, thus endorsing their specific status of risk factors-aware patients [Lambrinou E. Hansen T.B. Beulens J.W. Lifestyle factors, self-management and patient empowerment in diabetes care.]. Stronger associations emerged for improvements in physical activity, alcohol consumption and dietary habits, while diseases management and access to care were reported to suffer greatly.The distribution of the most well-known sociodemographic and lifestyle risk factors among people with diabetes is in line with the available literature, since type 2 diabetes mellitus incidence rises with age [Zheng Y. Ley S.H. Hu F.B. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications.] and is positively associated with high BMI and obesity [Lambrinou E. Hansen T.B. Beulens J.W. Lifestyle factors, self-management and patient empowerment in diabetes care.], lower educational levels [Mathisen J. Jensen A.K.G. Andersen I. Andersen G.S. Hvidtfeldt U.A. Rod N.H. Education and incident type 2 diabetes: quantifying the impact of differential exposure and susceptibility to being overweight or obese.] and lower self-reported socioeconomic status [Agardh E. Allebeck P. Hallqvist J. Moradi T. Sidorchuk A. Type 2 diabetes incidence and socio-economic position: a systematic review and meta-analysis.]. These latter act as risk factors both for the disease and worsened health outcomes, probably due to the lack of awareness and possibility of adopting proper lifestyle habits over time. Loneliness is also more common among people with diabetes [Hackett R.A. Hudson J.L. Chilcot J. Loneliness and type 2 diabetes incidence: findings from the english longitudinal study of ageing.], even though age might play a role. Loneliness increases vulnerability in older people who neglect healthy behaviours [Environmental/lifestyle factors in the pathogenesis and prevention of type 2 diabetes.], impacting psychological wellbeing. Anxiety [Anxiety and diabetes: innovative approaches to management in primary care.] and depressive symptoms [Environmental/lifestyle factors in the pathogenesis and prevention of type 2 diabetes.] usually scales scored higher values for people with diabetes, as we observed. The lower cigarettes consumption in people with diabetes may be a consequence of the diagnosis of diabetes and the consequent behavioural therapy set by the GP that discourages tobacco consumption, as confirmed by the higher rate of former smokers [Maddatu J. Anderson-Baucum E. Evans-Molina C. Smoking and the risk of type 2 diabetes.]. In contrast, the excess in alcohol consumption is a warning alarm, even more since alcohol has no nutritional value. They also engaged in nearly half as much physical activity as those not affected by chronic diseases, consistently with disease pathogenesis [Environmental/lifestyle factors in the pathogenesis and prevention of type 2 diabetes.], although inactivity is a primary risk factor for disease onset and progression.Consistently with general population, during pandemic BMI increased [Stival C. Lugo A. Bosetti C. Amerio A. Serafini G. Cavalieri d'Oro L. Odone A. Stuckler D. Iacoviello L. Bonaccio M. van den Brandt P.A. Zucchi A. Gallus S. COVID-19 confinement impact on weight gain and physical activity in the older adult population: data from the LOST in Lombardia study., Bakaloudi D.R. Barazzoni R. Bischoff S.C. Breda J. Wickramasinghe K. Chourdakis M. Impact of the first COVID-19 lockdown on body weight: a combined systematic review and a meta-analysis.], physical activity decreased [Stival C. Lugo A. Bosetti C. Amerio A. Serafini G. Cavalieri d'Oro L. Odone A. Stuckler D. Iacoviello L. Bonaccio M. van den Brandt P.A. Zucchi A. Gallus S. COVID-19 confinement impact on weight gain and physical activity in the older adult population: data from the LOST in Lombardia study., de Boer W.I.J. Mierau J.O. Schoemaker J. Viluma L. Koning R.H. The impact of the Covid-19 crisis on socioeconomic differences in physical activity behavior: evidence from the lifelines COVID-19 cohort study.] as sleep hours per night and sleep quality [Franceschini C. Musetti A. Zenesini C. Palagini L. Scarpelli S. Quattropani M.C. Lenzo V. Freda M.F. Lemmo D. Vegni E. Borghi L. Saita E. Cattivelli R. De Gennaro L. Plazzi G. Riemann D. Castelnuovo G. Poor sleep quality and its consequences on mental health during the COVID-19 lockdown in Italy.]. Psychiatric scales reported a worsening in depressive and anxiety symptoms [Amerio A. Lugo A. Stival C. Fanucchi T. Gorini G. Pacifici R. Odone A. Serafini G. Gallus S. COVID-19 lockdown impact on mental health in a large representative sample of Italian adults.]. Voluptuous habits displayed a non-significant reduction both in cigarettes/day and drinks/week (not among healthy individuals), as proved by previous inconsistent evidence [Carreras G. Lugo A. Stival C. Amerio A. Odone A. Pacifici R. Gallus S. Gorini G. Impact of COVID-19 lockdown on smoking consumption in a large representative sample of Italian adults., Schmidt R.A. Genois R. Jin J. Vigo D. Rehm J. Rush B. The early impact of COVID-19 on the incidence, prevalence, and severity of alcohol use and other

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