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Research Article| Volume 31, ISSUE 3, P802-813, March 10, 2021

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Trend of salt intake measured by 24-h urine collection in the Italian adult population between the 2008 and 2018 CUORE project surveys

Open AccessPublished:October 30, 2020DOI:https://doi.org/10.1016/j.numecd.2020.10.017

      Highlights

      • In Italian adults a significant reduction in salt intake has occurred over 10 years.
      • This reduction was independent of gender, age, BMI category and educational levels.
      • The salt intake in Italy remains definitely higher than recommended by WHO.
      • Salt intake remains higher in men, in overweight/obese and less education persons.

      Abstract

      Background and aims

      The WHO Global Action Plan for the Prevention of non-communicable diseases (NCDs) recommends a 30% relative reduction in mean population salt/sodium intake. The study assessed the trend in the habitual salt intake of the Italian adult population from 2008 to 2012 to 2018–2019 based on 24-h urinary sodium excretion, in the framework of the CUORE Project/MINISAL-GIRCSI/MENO SALE PIU’ SALUTE national surveys.

      Methods and results

      Data were from cross-sectional surveys of randomly selected age and sex–stratified samples of resident persons aged 35–74 years in 10 (out of 20) Italian Regions distributed in North, Centre and South of the Country. Urinary sodium and creatinine measurements were carried out in a central laboratory. The analyses included 942 men and 916 women examined in 2008–2012, and 967 men and 1010 women examined in 2018–2019. The age-standardized mean daily population salt (sodium chloride) intake was 10.8 g (95% CI 10.5–11.1) in men and 8.3 g (8.1–8.5) in women in 2008–2012 and respectively 9.5 g (9.3–9.8) and 7.2 g (7.0–7.4) in 2018–2019. A statistically significant (p<0.0001) salt intake reduction was thus observed over 10 years for both genders, and all age, body mass index (BMI) and educational classes.

      Conclusions

      The average daily salt intake of the Italian general adult population remains higher than the WHO recommended level, but a significant reduction of 12% in men and 13% in women has occurred in the past ten years. These results encourage the initiatives undertaken by the Italian Ministry of Health aimed at the reduction of salt intake at the population level.

      Keywords

      Introduction

      Non-communicable diseases (NCDs) are the main cause of death in all industrially developed countries [
      WHO
      Global action plan for the prevention and control of noncommunicable diseases 2013-2020.
      ]. Unhealthy life styles such as tobacco use, physical inactivity, inadequate diets and harmful use of alcohol all increase the risk of NCDs [
      WHO
      Global action plan for the prevention and control of noncommunicable diseases 2013-2020.
      ]. Creating environmental conditions that favour sustainable healthy habits is a fundamental tool to prevent and control NCDs. The WHO Global NCDs Action Plan 2013–2020 focussed on nine global targets and indicated a roadmap of policies and interventions useful to meet the commitments on NCD prevention made at the United Nations General Assembly in 2011 and 2014 and included in the 2030 Agenda for Sustainable Development [
      WHO
      Global action plan for the prevention and control of noncommunicable diseases 2013-2020.
      ].
      The Global Burden of Disease Risk Factors Collaboration estimated that 4.1 million annual deaths are attributable to excess salt/sodium intake mainly because of its impact on the incidence of hypertension, coronary heart disease and stroke [
      GBD 2015 Risk Factors Collaborators
      Global, Regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015.
      ]. Decreasing sodium intake has been shown to reduce blood pressure and the risk of associated cardiovascular disease [
      WHO. Prevention of Cardiovascular Disease
      Guidelines for assessment and management of cardiovascular risk.
      ,
      WHO
      Prevention of recurrent heart attacks and strokes in low and middle income populations: evidence-based recommendations for policy makers and health professionals.
      ,
      • Bibbins-Domingo K.
      • Chertow G.M.
      • Coxson P.G.
      • Lightwood J.M.
      • Pletcher M.J.
      • Goldman L.
      • et al.
      Projected effect of dietary salt reductions on future cardiovascular disease.
      ,
      • Cohen H.W.
      • Hailpern S.M.
      • Fang J.
      • Alderman M.H.
      Sodium intake and mortality in the NHANES II follow-up study.
      ,
      • Cutler J.A.
      • Follmann D.
      • Allender P.S.
      Randomized trials of sodium reduction: an overview.
      ] and has been identified as one of the most cost-effective measures countries can take to improve population health. A 30% relative reduction in the mean population salt intake by 2025 was indicated as one of the nine NCD-related global targets [
      WHO
      Global action plan for the prevention and control of noncommunicable diseases 2013-2020.
      ].
      In Italy, since 2008, the Ministry of Health, within the framework of the “Gaining Health: making healthy choices easy” strategic Programme for NCDs prevention, has launched specific initiatives, with the collaboration of the Interdisciplinary Working group for Salt Reduction in Italy (GIRCSI), aimed at the reduction excess salt intake [
      • Donfrancesco C.
      • Ippolito R.
      • Lo Noce C.
      • Palmieri L.
      • Iacone R.
      • Russo O.
      • et al.
      Excess dietary sodium and inadequate potassium intake in Italy: results of the MINISAL study.
      ,
      • Strazzullo P.
      • Cairella G.
      • Campanozzi A.
      • Carcea M.
      • Galeone D.
      • Galletti F.
      • et al.
      Population based strategy for dietary salt intake reduction: Italian initiatives in the European framework.
      ]. Furthermore, the reduction in excessive salt consumption is one of the main objectives of the National Preventive Plan (NPP) 2014–2018, extended to 2019, pursued at the Regional and local level.
      An assessment of the habitual salt intake was carried out in 2008–2012 in the Italian general population aged 35–74 years using 24-h urine collections obtained from the participants of the Osservatorio Epidemiologico Cardiovascolare/Health Examination Survey (OEC/HES 2008–2012) within the CUORE Project [
      • Giampaoli S.
      • Palmieri L.
      • Donfrancesco C.
      • Lo Noce C.
      • Pilotto L.
      • Vanuzzo D.
      For the Osservatorio Epidemiologico cardiovascolare/health examination survey research group. Cardiovascular health in Italy. Ten-year surveillance of cardiovascular diseases and risk factors: Osservatorio Epidemiologico cardiovascolare/health examination survey 1998-2012.
      ]. To evaluate the effectiveness of the salt reduction population strategy implemented by the Italian Ministry of Health in collaboration with non-governmental organizations, a further assessment of the adult population salt intake has been made in 2018–2019 (HES 2018–2019 – CUORE Project) to evaluate the trend in salt intake over the past ten years. Both studies were promoted and supported by the Italian Ministry of Health.

      Methods

      Study population

      Habitual salt intake comparison between OEC/HES 2008–2012 and HES 2018–2019 data for the purpose of the present analysis included persons aged 35–74 years, residents in 10 Regions involved in both surveys: Lombardy, Piedmont, Liguria, Emilia Romagna, Tuscany, Lazio, Abruzzo, Basilicata, Calabria and Sicily.
      From March 2008 to July 2012, the OEC/HES, within the CUORE Project, investigated randomly selected age and sex–stratified samples of 220 men and women aged 35–79 years per every 1.5 million residents in all Italian Regions. The participation rate of OEC/HES 2008–2012, defined as the number of persons who participated in the survey after receiving the invitation divided by the size of the eligible sample, was 53% [
      • Giampaoli S.
      • Palmieri L.
      • Donfrancesco C.
      • Lo Noce C.
      • Pilotto L.
      • Vanuzzo D.
      For the Osservatorio Epidemiologico cardiovascolare/health examination survey research group. Cardiovascular health in Italy. Ten-year surveillance of cardiovascular diseases and risk factors: Osservatorio Epidemiologico cardiovascolare/health examination survey 1998-2012.
      ]. In this framework, for the assessment of the population salt intake, the MINISAL-GIRCSI Study and MENO SALE PIU’ SALUTE Study used for each Region a randomly selected subsample of 100 men and 100 women aged 35–74 years, stratified by age and sex, based on the WHO recommendation that a sample of 100–200 individuals is required to estimate sodium intake with a 95% confidence interval (CI) about the mean of consumption of ±12 mmol/day using a single 24-h urine collection [
      WHO
      Reducing salt intake in populations: report of a WHO forum and technical meeting.
      ].
      The OEC/HES 2008–2012 was conducted by the Italian National Institute of Health (Istituto Superiore di Sanità – ISS) in collaboration with a national scientific association of cardiologists (ANMCO–Associazione Nazionale Medici Cardiologi Ospedalieri) and its foundation [Fondazione per il Tuo Cuore – Heart Care Foundation (HCF)]. The MINISAL-GIRCSI and MENO SALE PIU’ SALUTE studies were conducted by the ISS for the part referring to the adult population that is included in the present analysis, in collaboration with the Federico II University of Naples Department of Clinical and Experimental Medicine, which had the responsibility of the overall MINISAL-GIRCSI Study.
      From April 2018 to December 2019, a new HES has been conducted by the ISS, which has included the assessment of the Italian general adult population salt intake carried out in collaboration with Federico II University of Naples Department of Clinical Medicine and Surgery. The new survey investigated randomly selected age and sex–specific samples of 100 men and 100 women aged 35–74 years resident in 10 Regions (out of 20) chosen in the North, Centre and South of Italy. The participation rate of HES 2018–2019 was 40%.
      The 2008–2012 and 2018–2019 surveys were approved by the Ethical Committee of the ISS respectively on 11 November 2009 and 14 March 2018, and are recognized within the European Health Examination Survey collaboration [

      European Health Examination Survey (EHES) – Measuring the health of Europeans. http://www.ehes.info/national/national_hes_status.htm (accessed 19 September 2020).

      ].

      Study procedures and methods

      Both surveys included a 24-h urine collection, a physical examination and the administration of a common face-to-face questionnaire to collect information on demographic characteristics, educational level, lifestyles (physical activity, smoking, alcohol consumption, salt consumption), pathological history, family history and drug treatments. Standardized methods were used in the collection and measurement following European Health Examination Survey (EHES) recommendations [
      • Giampaoli S.
      • Palmieri L.
      • Donfrancesco C.
      • Lo Noce C.
      • Pilotto L.
      • Vanuzzo D.
      For the Osservatorio Epidemiologico cardiovascolare/health examination survey research group. Cardiovascular health in Italy. Ten-year surveillance of cardiovascular diseases and risk factors: Osservatorio Epidemiologico cardiovascolare/health examination survey 1998-2012.
      ,

      European Health Examination Survey (EHES) – Measuring the health of Europeans. http://www.ehes.info/national/national_hes_status.htm (accessed 19 September 2020).

      ] Persons were invited to enrol by postal letter and an information notice of the project made the participant informed about the research purposes and able to consciously sign an informed consent to participate.
      To assess dietary salt intake, participants were asked to collect all urines they passed during a 24-h period starting from the second morning urine pass and ending with the first urine passed the following morning. They were provided with a SARSTED plastic container of 3 L with the addition of thymol to prevent bacterial growth. Once the collection was returned, the total volume of urine was recorded and urine specimens were extracted after shaking. The specimens were immediately frozen: during the HES 2008–2012, three of them were kept at −30 °C for the measurement of sodium and creatinine whereas another one was maintained at −80 °C in the biological bank of the ISS for future determinations; during the HES 2018–2019, one at −30 °C and two at −80 °C respectively. The response rates to the request to provide 24-h urine samples among those who participated in the surveys were 92% in 2008–2012 and 99% in 2018–2019.
      The measurement of sodium and creatinine was performed for both surveys at Federico II University of Naples by the central laboratory of Department of Clinical and Experimental Medicine (later become Department of Clinical Medicine and Surgery). In each survey, both urinary sodium and creatinine concentrations were measured using an ABX Pentra 400 apparatus (HORIBA ABX, Rome, Italy) with an integrated ion-selective electrode (ISE) module. Sodium was measured by ion-selective electrode potentiometry using as urine-specific reference the Urichem Gold Bio Dev (Milan, Italy). Urinary creatinine was measured by a kinetic Jaffe’ reaction using as urine reference the Urichem Gold Bio Dev (Milan, Italy) in the 2008–2012 survey and the Low-and High Control ABX (Montpellier, France) in the 2018–2019 survey. Quality control data for the 2008–2012 survey were: accuracy −0.1% for sodium and −1.95% for creatinine, inter-assay variation coefficient 2.2% for sodium and 1.5% for creatinine and intra-assay variation coefficient 0.7% for sodium and 1.1% for creatinine. The respective data for the 2018–2019 survey were: accuracy −0.0% for sodium and −0.7% for creatinine, inter-assay variation coefficient 1.4% for sodium and 2.7% for creatinine and intra-assay variation coefficient 1.3% for sodium and 3.8% for creatinine. Pre-defined criteria for a high likelihood of incomplete urine collection were set as a 24-h urine volume below 500 ml or a creatinine content referred to body weight outside the range given by the population mean ± 2 standard deviations: based on these criteria, 122 participants were excluded from the analysis for the 2008–2012 and 104 participants for the 2018–2019 survey.
      The persons’ weight and height were measured while they were clothed only in their underwear. A balance beam scale was used for weight measurements, and height was measured with a height rule. Educational level and salt related habits were investigated through a face-to-face standardized questionnaire. A complete description of standardized methods and procedures of the OEC/HES 2008–2012 has been provided apart [
      • Giampaoli S.
      • Palmieri L.
      • Donfrancesco C.
      • Lo Noce C.
      • Pilotto L.
      • Vanuzzo D.
      For the Osservatorio Epidemiologico cardiovascolare/health examination survey research group. Cardiovascular health in Italy. Ten-year surveillance of cardiovascular diseases and risk factors: Osservatorio Epidemiologico cardiovascolare/health examination survey 1998-2012.
      ]. Similar procedures and methods were used for data collection in the HES 2018–2019 survey.

      Statistical analysis

      Sodium was expressed in millimoles as 24-h urinary excretion and was translated to salt intake in grams per day (1 mmol = 23 mg of sodium), following the WHO suggestion to deliver, as salt intake indicator, the age-standardized mean population intakes of salt expressed as g/day in order to allow comparisons among studies [
      WHO
      Global action plan for the prevention and control of noncommunicable diseases 2013-2020.
      ]. Sodium excretion (mmol) was multiplied by 23 to obtain sodium intake (g/day) which was further multiplied by 2.5 to obtain salt intake (g/day). For the assessment of this indicator, age-standardization was performed using the direct method referring to the age and sex–specific distributions of Italian adult population 2010 and 2019, respectively for OEC/HES 2008–2012 and HES 2018–2019 [
      National Institute of Statistics
      Resident population.
      ,
      National Institute of Statistics
      Resident population.
      ]. According to the WHO recommendation, the EFSA scientific opinion for sodium and the Standard Dietary Target for prevention in Italy [
      WHO
      Guideline: sodium intake for adults and children.
      ,
      European Food Safety Authority
      Dietary reference values for sodium. Adopted.
      ,
      SINU, the Italian Society of Human Nutrition
      Recommended intake levels of energy and nutrients for the Italian population.
      ] the prevalence of 24-h sodium excretion lower than 85 mmol (corresponding to 5 g of salt) per day was calculated.
      Salt intake was also assessed by four classes of age (35–44, 45–54, 55–64 and 65–74 years) and, for those with available information, by three classes of body mass index (BMI; weight in kilogram divided by height in square metres) (normal weight – BMI within 18.5–24.9 kg/m2, overweight BMI within 25.0–29.9 kg/m2 and obesity BMI ≥ 30 kg/m2) and two classes of educational level (higher education – high school or college, lower education – primary or middle school). The results are expressed as means and standard deviations for quantitative variables and prevalence for qualitative ones; the related 95% CIs are reported. The t-test for unpaired samples (for equal or unequal variance as appropriate) or analysis of variance (ANOVA) was used to assess differences between group means. The chi-square test was used to compare prevalence. Two-sided p-values less than 0.05 were considered statistically significant. Statistical analyses were performed using the SAS software, release 9.4 (SAS Institute Inc, Cary, NC).

      Results

      After the exclusions reported above due to possibly incomplete urine collections, 942 men and 916 women (mean age ± std.: men 54 ± 11 and women 55 ± 11) and 967 men and 1010 women (mean age ± std.: men 55 ± 11 and women 56 ± 11) were included in the analysis relative to the 2008–2012 and the 2018–2019 survey, respectively.
      Similar mean levels of 24-h urine volume as well as crude- and weight-adjusted creatinine were found in the two surveys by age class and gender (Table S1). The mean level of crude urinary creatinine excretion was higher in men than in women within both periods in each age class (p-value<0.0001). Moreover, in both periods, a progressively lower crude- and weight-adjusted creatinine excretion rate was found with age (p-value<0.0001). A trend was also observed towards a higher urine volume with age (Table S1).
      In the 2008–2012 survey, mean 24-h urinary sodium excretion was 186 mmol (95% CI 181–190) in men and 143 mmol (139–146) in women; in the 2018–2019 survey, the respective values were 164 (160–168) and 124 (121–127) (Fig. 1). The mean sodium excretion was significantly reduced from 2008 to 2012 to 2018–2019 in both men (−12%) and women (−13%) (p-value<0.0001); the reduction was statistically significant in all age classes (Table 1).
      Figure 1
      Figure 1Frequency distribution of 24-h urinary sodium excretion by gender and period in Italy. Men and women aged 35–74 years, CUORE Project health examination surveys 2008–2012 and 2018–2019.
      Table 1Data on 24-h sodium excretion (mmol) by sex, age class and period in Italy. Men and women aged 35–74 years, CUORE Project health examination surveys 2008–2012 and 2018–2019.
      Age class (years)2008201220182019% mean difft-test p-value
      nmeanstd95% CIANOVA p-valuenmeanstd95% CIANOVA p-value
      MEN
      0.45990.7640
      35442351857217619422816266154171−120.0004
      45542381916818219923216763159176−120.0001
      55642401877517819726616360156170−130.0001
      65742291806817218924116259155170−100.0023
      WOMEN
      0.18990.0936
      35442201435613515021312147115127−15<0.0001
      45542231496214115725212347117129−17<0.0001
      55642411415013514827513055124137−80.0156
      65742321385413114527012146115126−120.0002
      t-test: normal standardized t-test for comparison between periods.
      Italian Regions: Lombardy, Piedmont, Liguria, Emilia Romagna, Tuscany, Lazio, Abruzzo, Basilicata, Calabria and Sicily.
      ANOVA: ANOVA to compare 24 h sodium excretion among age classes within the period.
      The age-standardized mean population salt intake was 10.8 g (standard deviation 4.1; 95% CI 10.5–11.1) in men and 8.3 g (3.2; 8.1–8.5) in women in the 2008–2012 survey and 9.5 g (3.6; 9.3–9.8) in men and 7.2 g (2.8; 7.0–7.4) in women in the 2018–2019 survey; the reduction by period was equal to 1.3 g in men and 1.1 g in women (p < 0.0001 for both).
      Frequency distributions of 24-h urinary sodium excretion are shown in Fig. 1. Sodium excretion was consistently higher in men than in women, with a difference of 23% (p-value< 0.0001) in 2008–2012 and 24% in 2018–2019 (p-value<0.0001). Within period, no statistically significant differences were found for the mean of 24-h urinary sodium excretion across age classes (ANOVA, Table 1).
      In the 2008–2012 survey, 24-h sodium excretion was lower than 85 mmol per day, in 4% (95% CI 3–5%) of men and 15% (13–17%) of women; in the 2018–2019 survey significantly higher values of 9% (7–11%) and 23% (20–26%) were found for men and women (p-value<0.0001).
      In both periods and genders, 24-h sodium excretion was significantly and directly associated with BMI classes and inversely associated with educational levels, independently of age (ANOVA within period – Table 2).
      Table 2Data on 24-h sodium excretion (mmol) by sex, body mass index class, educational level and period in Italy. Men and women aged 35–74 years, CUORE Project health examination surveys 2008–2012 and 2018–2019.
      2008–20122018–2019% mean difft-test p-valueANOVA between periods p-value
      nmeanstd95% CIANOVA within period p-valuenmeanstd95% CIANOVA within period p-value
      MEN
      Body mass index<0.0001<0.0001<0.0001
      Normal weight2351706416217831414754141153−14<0.0001
      Overweight4541826717618945816863163174−80.0013
      Obese2462097919921919118263173191−130.0001
      Education0.01950.0003<0.0001
      Higher education4971817217518768515958155164−12<0.0001
      Lower education4361916918519827917570167183−90.0020
      Period<0.0001
      WOMEN
      Body mass index<0.0001<0.0001<0.0001
      Normal weight3611294912413444311445110119−12<0.0001
      Overweight2991435113814929913052124136−90.0017
      Obese2461616415316925013550129141−16<0.0001
      Education0.00530.0063<0.0001
      Higher education4551375513214368512147117124−12<0.0001
      Lower education4471475514215232313052124136−11<0.0001
      Period<0.0001
      Body mass index was available in 941 men and 916 women for the 2008–2012 survey and 967 men and 1010 women for 2018–2019 survey.
      Educational level was available in 933 men and 902 women for the 2008–2012 survey and 964 men and 1008 women for 2018–2019 survey.
      t-test: normal standardize t-test for comparison between periods. ANOVA within period: ANOVA p-value of the corresponding variable to compare 24 h sodium excretion among age classes (35–44, 45–54, 55–64 and 65–74 years), body mass index classes and educational levels. ANOVA between periods: ANOVA p-value of the corresponding variable to compare 24 h sodium excretion among periods, age classes (35–44, 45–54, 55–64 and 65–74 years), body mass index classes and educational levels. ANOVA analyses were performed among those with BMI ≥ 18.5 kg/m2. Normal weight – body mass index-BMI within 18.5–24.9 kg/m2, overweight BMI within 25.0–29.9 kg/m2 and obesity BMI≥30 kg/m2. Higher education – high school or college; lower education – primary or middle school. Italian regions: Lombardy, Piedmont, Liguria, Emilia Romagna, Tuscany, Lazio, Abruzzo, Basilicata, Calabria and Sicily.
      The statistically significant reduction of 24-h sodium excretion between 2008–2012 and 2018–2019 was consistent across BMI classes and educational levels, considered singly (t-test –Table 2) or together independently of age (period significance of ANOVA between periods – Table 2).
      In both periods, some geographical differences were found for 24-h sodium excretion independently of age, BMI and educational classes (Table S2); no Region had mean levels within those recommended (lower than 85 mmol) (Table S2 and Fig. 2) but a trend to reduction was observed between the two surveys in all Regions (except for men in the Abruzzo Region) (Table S2).
      Figure 2
      Figure 2Mean of 24-h urinary sodium excretion by gender, period and Region in Italy. Men and women aged 35–74 years, CUORE Project health examination surveys 2008–2012 and 2018–2019.
      A trend to an increased prevalence of healthy salt–related habits was also observed between 2008–2012 and 2018–2019: in the second survey there was a higher proportion of men and women who reportedly never or rarely add salt at table, who eat always or very often bread without salt and who taste as more salty the food consumed out of home (Fig. 3). Nevertheless, in the 2018–2019 survey as many as 80% of men and 77% of women declared to be not influenced from the salt content information on food labels while shopping (data not available in the 2008–2012 survey) (Fig. 3).
      Figure 3
      Figure 3Prevalence (%) of self-reported salt-related habits by gender and period in Italy. Men and women aged 35–74 years, CUORE Project health examination surveys 2008–2012 and 2018–2019.

      Discussion

      The main finding of the present study is the observation of a significant reduction of the habitual salt intake in randomly selected samples of general adult population recruited in ten Italian Regions approximately ten years apart. The reduction was detected to different extents in almost all Regions and was consistent with respect to sex, age, BMI category and education level.
      The second important finding however was that the average daily salt intake remains largely higher than the level recommended by WHO and taken as the Standard Dietary Target for the Italian population: this is also true in all the surveyed Regions, for both men and women, and all age classes, education levels and BMI categories.
      A significant trend of habitual salt intake reduction had never been observed in Italy: previously available information on dietary salt intake from several local studies such as the 1976 study of households, the 1985–1987 Intersalt (Gubbio, Bassiano, Mirano, Naples), the 1991 and the 2002–2004 Olivetti Heart Study showed approximately similar levels, not far from those observed within the OEC/HES 2008–2012 survey, considering similar geographical areas [
      • Donfrancesco C.
      • Ippolito R.
      • Lo Noce C.
      • Palmieri L.
      • Iacone R.
      • Russo O.
      • et al.
      Excess dietary sodium and inadequate potassium intake in Italy: results of the MINISAL study.
      ,
      • Strazzullo P.
      • Trevisan M.
      • Farinaro E.
      • Cappuccio F.P.
      • Ferrara L.A.
      • Mancini M.
      Characteristics of the association between salt intake and blood pressure in a sample of male working population in southern Italy.
      ,
      Intersalt Cooperative Research Group
      Intersalt: an interna- tional study of electrolyte excretion and blood pressure. Results for 24 hour urinary sodium and potassium excretion.
      ,
      • Leclercq C.
      • Ferro-Luzzi A.
      Total domestic consumption of salt and their determinants in three Regions of Italy.
      ,
      • Venezia A.
      • Barba G.
      • Russo O.
      • Capasso C.
      • De Luca V.
      • Farinaro E.
      • et al.
      Dietary sodium intake in a sample of adult male population in southern Italy: results of the Olivetti heart study.
      ].
      The average reduction in salt intake observed in adults within the HES 2018–2019 survey compared to the previous one (12% in men and 13% in women) is more than one-third of the 2025 WHO global target of a 30% relative reduction. The trend observed in our study is consistent with the trend to salt intake reductions recently reported for other countries, albeit with different methodologies for salt intake assessment. Thus, Slovenia (from 2007 to 2012), Turkey (from 2008 to 2012) and the UK (from 2001 to 2011) reported salt intake reductions of 9%, 17% and 15% respectively, based on 24-h urinary excretion [
      • Kathy T.
      • Bruce N.
      • Corinna H.
      • Dunford E.
      • Campbell N.
      • Rodriguez-Fernandez R.
      • et al.
      Salt reduction initiatives around the world – a systematic review of progress towards the global target.
      ,
      World Health Organization
      Progress in reducing salt consumption in Turkey.
      ,
      • Sadler K.
      • Nicholson S.
      • Steer T.
      • Gill V.
      • Bates B.
      • Tipping S.
      • et al.
      National diet & nutrition survey—assessment of dietary sodium in adults (aged 19 to 64 years) in England.
      ]. Finland monitored population salt intake through both 24-h urine collection and dietary surveys and reported a 36% reduction from 1979 to 2007 [
      • Pietinen P.
      • Paturi M.
      • Reinivuo H.
      • Tapanainen H.
      • Valsta L.M.
      FINDIET 2007 Survey: energy and nutrient intakes.
      ]. Using spot urine collections, Denmark reported a 7% decrease from 2006 to 2010 [
      European Commission
      National salt initiatives: implementing the EU framework for salt reduction activities.
      ,
      • Thuesen H.B.
      • Toft U.
      • Buhelt L.P.
      • Linneberg A.
      • Friedrich N.
      • Nauck M.
      • et al.
      Estimated daily salt intake in relation to blood pressure and blood lipids: the role of obesity.
      ]. Dietary surveys were used by France (1999.2007), Iceland (1999–2007) and Ireland (2001–2011), which reported reductions of 5%, 6% and 14%, respectively [
      European Commission
      Collated information on salt reduction in the EU.
      ,
      World Health Organization
      Mapping salt reduction initiatives in the WHO European Region.
      ,
      • Walton J.
      Salt intakes in the Irish population: estimates and trends.
      ]. Among non-European countries, China (from 1991 to 2009), Japan (from 1997 to 2012), Korea (from 2005 to 2012) and South Korea (from 2010 to 2014) reported reductions of 29%, 23%, 14% and 20%, respectively [
      • Kathy T.
      • Bruce N.
      • Corinna H.
      • Dunford E.
      • Campbell N.
      • Rodriguez-Fernandez R.
      • et al.
      Salt reduction initiatives around the world – a systematic review of progress towards the global target.
      ,
      • Du S.
      • Neiman A.
      • Batis C.
      • Wang H.
      • Zhang B.
      • Zhang J.
      • et al.
      Understanding the patterns and trends of sodium intake, potassium intake, and sodium to potassium ratio and their effect on hypertension in China.
      ,
      • Hye-Kyung P.
      • Yoonna L.
      • Baeg-Won K.
      • Kwon K.
      • Jong-Wook K.
      • Kwon O.
      • et al.
      Progress on sodium reduction in South Korea.
      ].
      However, a few countries have reported increase in the population habitual salt intake, such as Iran, USA and India [
      • Mohammadifard N.
      • Khosravi A.
      • Salas-Salvadó J.
      • Becerra-Tomás N.
      • Nouri F.
      • Abdollahi Z.
      • et al.
      Trend of salt intake measured by 24-hour urine collection samples among Iranian adults population between 1998 and 2013: the Isfahan salt study.
      ,
      • Pfeiffer C.M.
      • Hughes J.P.
      • Cogswell M.E.
      • Burt V.L.
      • Lacher D.A.
      • Lavoie D.J.
      • et al.
      Urine sodium excretion increased slightly among U.S. adults between 1988 and 2010.
      ,
      • Johnson C.
      • Praveen D.
      • Pope A.
      • Raj T.S.
      • Pillai R.N.
      • Land M.A.
      • et al.
      Mean population salt consumption in India: a systematic review.
      ].
      Additional findings of the present study are the sex-related difference in salt intake and the statistical associations of salt intake with BMI and educational level. All these findings are confirmatory of previous evidence. The gender difference is likely explained by differences in food and energy intake between men and women. The association between sodium excretion and BMI was also found in the preliminary report on the MINISAL Study [
      • Donfrancesco C.
      • Ippolito R.
      • Lo Noce C.
      • Palmieri L.
      • Iacone R.
      • Russo O.
      • et al.
      Excess dietary sodium and inadequate potassium intake in Italy: results of the MINISAL study.
      ] and is also consistent with previous evidence from the Olivetti Heart Study [
      • Venezia A.
      • Barba G.
      • Russo O.
      • Capasso C.
      • De Luca V.
      • Farinaro E.
      • et al.
      Dietary sodium intake in a sample of adult male population in southern Italy: results of the Olivetti heart study.
      ] and with data from many other countries [
      • Venezia A.
      • Barba G.
      • Russo O.
      • Capasso C.
      • De Luca V.
      • Farinaro E.
      • et al.
      Dietary sodium intake in a sample of adult male population in southern Italy: results of the Olivetti heart study.
      ,
      • Ortega R.M.
      • Lopez-Sobaler A.M.
      • Ballesteros J.M.
      • Pérez-Farinós N.
      • Rodríguez-Rodríguez E.
      • Aparicio A.
      • et al.
      Estimation of salt intake by 24 h urinary sodium excretion in a representative sample of Spanish adults.
      ,
      • Oh S.W.
      • Koo H.S.
      • Han K.H.
      • Han S.Y.
      • Chin H.J.
      Associations of sodium intake with obesity, metabolic disorder, and albuminuria according to age.
      ,
      • Lee J.
      • Hwang Y.
      • Kim K.N.
      • Ahn C.
      • Sung H.K.
      • Ko K.P.
      • et al.
      Associations of urinary sodium levels with overweight and central obesity in a population with a sodium intake.
      ,
      • Khosravi A.
      • Toghianifar N.
      • Sarrafzadegan N.
      • Gharipour M.
      • Azadbakht L.
      Salt intake, obesity, and pre-hypertension among Iranian adults: a cross-sectional study.
      ,
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      • Noori F.
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      • et al.
      Is the association between salt intake and blood pressure mediated by body mass index and central adiposity?.
      ,
      • Yi S.S.
      • Firestone M.J.
      • Beasley J.M.
      Independent associations of sodium intake with measures of body size and predictive body fatness.
      ,
      • Zhang X.
      • Wang J.
      • Li J.
      • Yu Y.
      • Song Y.
      A positive association between dietary sodium intake and obesity and central obesity: results from the National Health and Nutrition Examination Survey 1999-2006.
      ,
      • Lydon R.
      • McAnena L.
      • Livingstone M.
      • Kerr M.
      The association between salt intake and obesity in UK adults aged 19–64 years.
      ]. A possible explanation in this case is that foods with high sodium content are also usually high in energy, such as fatty and highly processed foods [
      • Bolhuis D.P.
      • Lakemond C.M.
      • de Wijk R.A.
      • et al.
      Effect of salt intensity in soup on ad libitum intake and onsubsequent food choice.
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      Association between intake of nutrients and food groups and liking for fat (The Nutrinet-Sante Study).
      ], leading to weight gain [
      • Keskitalo K.
      • Tuorila H.
      • Spector T.D.
      • Cherkas L.F.
      • Knaapila A.
      • Kaprio J.
      • et al.
      The Three-Factor Eating Questionnaire, bodymass index, and responses to sweet and salty fatty foods: atwin study of genetic and environmental associations.
      ].
      The inverse association between salt intake and educational level was already reported by the OEC/HES 2008–2012 survey on 20 Italian Regions, showing that social inequalities, including disparities in the educational level, explained the geographical variation in salt intake in our country [
      • Cappuccio F.P.
      • Ji C.
      • Donfrancesco C.
      • Palmieri L.
      • Ippolito R.
      • Vanuzzo D.
      • et al.
      Geographic and socioeconomic variation of sodium and potassium intake in Italy: results from the MINISAL-GIRCSI programme.
      ]. This finding was consistent with evidence from a recent systematic review and meta-analysis that included cohorts from high-income countries of East Asia, Australia, North America, Europe and Latin America [
      • de Mestral C.
      • Mayén A.L.
      • Petrovic D.
      • Marques-Vidal P.
      • Bochud M.
      • Stringhini S.
      Socioeconomic determinants of sodium intake in adult populations of high-income countries: a systematic review and meta-analysis.
      ]. In this case too it is conceivable that less educated people consume relatively greater amounts of possibly cheaper fatty and highly processed foods with high sodium content and high caloric density [
      • Darmon N.
      • Drewnowski A.
      Does social class predict diet quality?.
      ,
      • Novakovíc R.
      • Cavelaars A.
      • Geelen A.
      • et al.
      Socioeconomic determinants of micronutrient intake and status in Europe: a systematic review.
      ,
      • Wang D.D.
      • Leung C.W.
      • Li Y.
      • Ding E.L.
      • Chiuve S.E.
      • Hu F.B.
      • et al.
      Trends in dietary quality among adults in the United States, 1999 through 2010.
      ,
      • Nikolíc M.
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      • Gurinovíc M.
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      • Khokhar S.
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      • et al.
      Identifying critical nutrient intake in groups at risk of poverty in Europe: the CHANCE project approach.
      ,
      WHO
      A global brief on hypertension: silent killer, global public health crisis.
      ]. It is also possible that the educational level impacts on the way people are responsive to health information with a greater propensity of more educated individuals to comply with nutritional advice. It is to be noted however that in our study the reduction in salt intake over the past 10 years was similar for higher and lower educational levels, with only a minor difference in men. These results may suggest that salt consumption among Italian adults benefited from preventive actions that have reached the population across the board, such as agreements between the Italian Ministry of Health and associations of artisan bakers and companies in the food industry aimed at reducing salt content in artisan and industrial bread and in some industrial products (pasta, rice, soups) and the actions developed by all the Italian Regions with the National Prevention Plan 2014–2019, recently renewed and strengthened for 2020–2025 [
      • Strazzullo P.
      • Cairella G.
      • Campanozzi A.
      • Carcea M.
      • Galeone D.
      • Galletti F.
      • et al.
      Population based strategy for dietary salt intake reduction: Italian initiatives in the European framework.
      ]. The agreements provided for a relative reduction of the salt content of 10–15%, depending on products and association/manufactures. Initiatives included in the National Prevention Plan, such as local intersectoral agreements and information activities for the population and training for operators related to the food sector, were followed by specific monitoring systems of the Regional Prevention Plans. These preventive programmes have been supported by the advocacy actions and the educational campaigns promoted at regular intervals by scientific societies.
      In accordance with the trend in salt intake, the findings of the questionnaire on the population's life style habits related to salt intake showed an overall substantial improvement, although it is a matter of concern the modest attention paid to food labels concerning the salt content of foods when shopping.

      Strengths and limitations

      Major strengths of our study are as follows: the use of the gold standard method for the assessment of salt intake at the population level; the good national coverage with enrolment of the study participants through random age and sex stratification in half of the Italian Regions distributed in Northern, Central and Southern Italy; the excellent compliance with the request to provide 24-h urines; the overall good quality of the urine collections as indicated by the large mean urinary volume and by the finding of the expected mean values for urinary creatinine with the physiological differences related to sex, age and body weight.
      However, we acknowledge some study limitations which should be considered when interpreting our results. First, because of the choice of urban districts for the random selection of the study participants in both surveys, the results may not be representative of the habits of populations living in rural areas. The participation rates to the surveys were lower than desirable, yet consistent with lower contact rates occurring in more highly urbanized areas and with the decreasing trend of participation observed in health examination surveys in other European countries [
      • Mindell J.S.
      • Giampaoli S.
      • Goesswald A.
      • et al.
      Sample selection, recruitment and participation rates in health examination surveys in Europe--experience from seven national surveys.
      ] and anyway within the WHO recommended sample size for this kind of epidemiological investigations [
      WHO
      Reducing salt intake in populations: report of a WHO forum and technical meeting.
      ]. The cross-sectional design of the study does not allow to assess causality of the associations between salt intake and BMI or educational level. The use of a single 24-h urine collection does not allow to accurately assess the individual salt intake due to the well-known large day-to-day variation in sodium excretion: however, it is sufficient for the assessment of salt intake in adequately sized population groups. There were differences in the educational level distribution between the two surveys, which are consistent with the increase in secondary and tertiary education assessed in adults from 2008 to 2017 by the Italian National Institute of Statistics [
      Italian National Institute of Statistics
      Population education levels and occupational returns: the main indicators.
      ]. There was also some difference in the BMI distribution. Nevertheless, these differences cannot have affected our major findings because, both in men and women, the amount of salt reduction was similar by BMI classes and educational levels. Moreover, the reduction of mean salt intake between periods was statistically significant when adjusted by BMI class and educational level. Finally, the salt intake monitoring was not extended to the younger age classes.

      Conclusions

      In conclusion, this comparison of 24-h urinary sodium excretion in two independent samples of Italian adult population, carried out in 10 Regions approximately 10 years apart from each other, showed a significant and substantial reduction in salt intake. This reduction was independent of gender, age, BMI category and educational level and met more than one-third of the 30% reduction target indicated in the WHO Global Action Plan 2013–2020.
      This notwithstanding, the study indicated that the average salt intake in Italy remains definitely higher than the level recommended by WHO for both genders, all Regions and every class of age, BMI and educational level. Mean levels of salt intake were higher in men than in women, in those with overweight and obesity compared with normal-weight people, and in less educated compared with more educated individuals, confirming the important role of social inequalities.
      Although these results need confirmation through further systematic and periodic monitoring, they have major public health implications in as much as they encourage the initiatives undertaken by the Italian Ministry of Health in collaboration with non-governmental organizations and in particular with the scientific societies in order to reduce salt intake at the population level through the “Gaining Health: making healthy choices easy” Programme and the National Prevention Plan. The attainment of this initial success in the contrast to a major causal factor of NCDs should prompt further actions to lower the amount of salt in the food supply, to generate knowledge and improve people behaviours through educational campaigns targeting also children and adolescents, to change the food environment and promote social norms so that people demand and gain greater control over their salt consumption. As suggested by the WHO and in accordance with the Italian Ministry of Health population strategy developed since 2008, regular surveillance is needed to make sure that strategies are appropriately targeted and changes can be measured over time.

      Funding

      The Osservatorio Epidemiologico Cardiovascolare/Health Examination Survey OEC/HES 2008–2012 within the CUORE Project was funded by the Italian Ministry of Health (MoH), the Associazione Nazionale Medici Cardiologi Ospedalieri (ANMCO), the Fondazione per il Tuo cuore onlus (Heart Care Foundation – HCF) and the Joint Action of the European Health Examination Survey; the OEC/HES 2008–2012 included the MINISAL Study and part of the MENO SALE PIU’ SALUTE Study, promoted and funded by the MoH – National Center for Disease Prevention and Control (CCM). The HES 2018–2019 within the CUORE Project was promoted and funded by the MoH – CCM for activities related to the CCM 2017 project – Central Actions Area – entitled “Monitoring of the average daily consumption of sodium in the Italian population”. The OEC/HES 2008–2012 and HES 2018–2019 was also funded by the Italian National Institute of Health (Istituto Superiore di Sanità – ISS) through permanent staff salary and some travels refund.

      Author contributions

      CD participated in the study conception and design, managed the data collection and quality control, performed data analysis, interpreted results, drafted the manuscript and contributed to the management and storage of urine samples; CL contributed to the data collection, to quality control, to the management and the storage of urine samples and critically revised the manuscript; OR and RI performed the laboratory measurements, contributed to the data quality control and critically revised the manuscript; DM performed information technology services, contributed to the data collection and quality control and critically revised the manuscript; ADL contributed to data collection and quality control and critically revised the manuscript; EP contributed to data collection and critically revised; BB contributed to data collection and critically revised; FV contributed to information technology services and critically revised the manuscript; SV, FG, MMG, GO critically revised the manuscript; DG participated in the study conception, scientifically supported the studies and critically revised the manuscript; PB scientifically supported the studies and critically revised the manuscript; SG participated in the study conception and design, managed the data collection and quality control, contributed to the management and storage of urine samples and critically revised the manuscript; LP contributed to the storage of urine samples and critically revised the manuscript; PS participated in the study conception and design, was responsible for the laboratory measurements and data quality control, interpreted results and critically revised the manuscript. All authors have read and approved the final version of this manuscript for submission.

      Declaration of competing interest

      Authors have nothing to disclose.

      Acknowledgments

      Research Group of Osservatorio Epidemiologico Cardiovascolare/Health Examination Survey (OEC/HES) 2008–2012 within the CUORE Project for the National Institute of Health (Istituto Superiore di Sanità – ISS): Luigi Palmieri (coordinator), Chiara Donfrancesco (coordinator), Simona Giampaoli (former coordinator), Cinzia Lo Noce, Serena Vannucchi, Anna Di Lonardo, Francesco Dima (former). Research group of the CUORE Project OEC/HES 2008–2012 for Associazione Nazionale Medici Cardiologi Ospedalieri/Health Care Foundation (ANMCO/HCF): Michele Massimo Gulizia, Furio Colivicchi and Andrea Di Lenarda (coordinators), Diego Vanuzzo (former coordinator), Domenico Gabrielli, Giuseppe Di Pasquale, Aldo Pietro Maggioni, Gian Francesco Mureddu, Carmine Riccio, Marino Scherillo, Stefano Urbinati, Pompilio Faggiano. Local coordinators of the OEC/HES 2008–2012 participating centers: Diego Vanuzzo (Centro di Prevenzione Cardiovascolare ASS 4 “Medio Friuli”, Udine); Licia Iacoviello (Centro di ricerca e formazione ad alta tecnologia nelle scienze biomediche Giovanni Paolo II, Università Cattolica, Campobasso); Federico Vancheri (Ospedale S. Elia, Caltanissetta); Carlo Alberto Goldoni (Dipartimento di sanità pubblica, Azienda USL, Modena); Carmelo Antonio Caserta (Associazione calabrese di epatologia, Cittanova – Reggio Calabria); Antonio Lopizzo (Ospedale San Carlo, Potenza); Natalino Meloni (USL 4, Loceri – Nuoro); Marinella Gattone (Fondazione S. Maugeri, Veruno – Novara); Giuseppe Salamina (SC Centro controllo malattia, ASL TO1, Torino); Alessandro Boccanelli (Ospedale San Giovanni Addolorata, Roma); Roberto Amici (Ospedale Santa Maria della Pietà, Camerino -Macerata); Gianfranco Alunni (Ospedale SantaMaria della Misericordia, Azienda Ospedaliera, Perugia); Giuseppe Favretto (Ospedale rabilitativo di alta specializzazione, Motta di Livenza – Treviso); Mariapiera Vettori (Azienda ULSS 13 del Veneto, Noale – Venezia);Marino Scherillo (Azienda Ospedaliera G. Rummo, Benevento); Pompilio Faggiano (Azienda Ospedaliera Spedali Civili, Brescia); Maria Teresa La Rovere (Fondazione Salvatore Maugeri, Istituto di riabilitazione, Montescano – Pavia); Maria Luisa Biorci (ASL 3 Genovese- PO “La Colletta”, Arenzano – Genova); Pasquale Caldarola (Cardiologia, Ospedale di Terlizzi, Centro servizi territoriali della città, Bitonto – Bari); Giovanni Menegoni (Azienda provincial per i servizi sanitari di Trento, Presidio ospedaliero, Borgo Valsugana – Trento); Rosa Maria Teresa Cristaudo (Azienda USL della Valle d’Aosta, Aosta); Andrea Zipoli (Azienda USL 11, Ospedale San Giuseppe, Empoli – Firenze); Paolo Michele Accettura (Laboratorio analisi, Ospedale San Camillo, Atessa – Chieti). Administrative staff of the ANMCO/HCF: Giulia Salone, Angela Petrucci, Monica Nottoli; and to Laura Bellicini and to L Bellicini, consultant lawyer of the ANMCO-HCF. Fondazione IRCCS, Istituto nazionale dei tumori, Milano: Vittorio Krogh, Sara Grioni. Research Group MINISAL-GIRCSI and MENO SALE PIU′ SALUTE: Pasquale Strazzullo, Ornella Russo, Lanfranco D'Elia, Roberto Iacone, Renato Ippolito, Enrico Agabiti-Rosei, Angelo Campanozzi, Marina Carcea, Ferruccio Galletti, Licia Iacoviello, Luca Scalfi, Alfonso Siani, Daniela Galeone, Chiara Donfrancesco, Simona Giampaoli. CARHES Research Group: Luca De Nicola, Chiara Donfrancesco, Roberto Minutolo, Cinzia Lo Noce, Luigi Palmieri, Amalia De Curtis, Licia Iacoviello, Carmine Zoccali, Loreto Gesualdo, Giuseppe Conte, Diego Vanuzzo, Simona Giampaoli. Research Group of the Health Examination Survey (HES) 2018–2019 within the CUORE Project: Chiara Donfrancesco (coordinator), Luigi Palmieri, Cinzia Lo Noce, Daniela Minutoli, Anna Di Lonardo, Elisabetta Profumo, Brigitta Buttari, Serena Vannucchi, Simona Giampaoli (former coordinator) (Italian National Institute Health -Istituto Superiore di Sanità, ISS). Local referents of HES 2018–2019 partecipating centers: Luigi Dell’Orso and Alessandro Grimaldi (Ospedale San Salvatore, L'Aquila); Nicola Giordano (ASL – Azienda Sanitaria Locale di Potenza, Potenza); Carmelo Caserta (Centro di Medicina Solidale – Associazione Calabrese di Epatologia, Reggio Calabria); Alessandra Fabbri (Casa della Salute AUSL RE, Montecchio Emilia); Fabrizio Ciaralli (Casa della Salute S. Caterina della Rosa, Rome); Fiorella Bagnasco (Municipality of Arenzano, Arenzano – Genova); Giuliana Rocca (ATS Bergamo); Giuseppe Salamina (ASL Città di Torino, Torino); Pietro Modesti (Università di Firenze, Florence); Federico Vancheri and Giulio Geraci (Ospedale S. Elia, Caltanissetta). Also we would to thank for HES 2018–2019: Anna Rita Ciccaglione, Cinzia Marcantonio, Roberto Bruni (ISS), Emanuele Bottosso and Anna Acampora (as trainee medical doctor at ISS), Giulia Cairella (ASL Roma 2, SINU) and Municipality of Potenza. Italian Ministry of Health: Daniela Galeone, Paolo Bellisario, Giovanna Laurendi, Bianca Maria Polizzi. European Health Examination Survey, Reference Centre: Hanna Tolonen, Kari Kuulasmaa, Paivikki Koponen, Johan Heldan, Susanna Conti, Georg Alfthan. Administrative staff of the ISS: Claudia Meduri, Tiziana Grisetti, Matilde Bocci, Gabriella Martelli, Valerio Occhiodoro, Maria Grazia Carella, Francesca Romana Meduri.
      We acknowledge all persons who decided to participate in the OEC/HES 2008–2012 and HES 2018–2019 surveys.

      Appendix A. Supplementary data

      The following are the Supplementary data to this article:

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