Two-stage, school and community-based population screening successfully identifies individuals and families at high-risk for type 2 diabetes: the Feel4Diabetes-study

Yannis Manios, Christina Mavrogianni, Christina-Paulina Lambrinou, Greet Cardon, Jaana Lindström, Violeta Iotova, Tsvetalina Tankova, Fernando Civeira, Jemina Kivelä, Zoltán Jancsó, Samyah Shadid, Kaloyan Tsochev, Rocío Mateo-Gallego, Sándorné Radó, George Dafoulas, Konstantinos Makrilakis, Odysseas Androutsos, Feel4Diabetes-study group, Yannis Manios, Greet Cardon, Jaana Lindström, Peter Schwarz, Konstantinos Makrilakis, Lieven Annemans, Ignacio Garamendi, Meropi Kontogianni, Odysseas Androutsos, Christina Mavrogianni, Konstantina Tsoutsoulopoulou, Christina Katsarou, Eva Karaglani, Irini Qira, Efstathios Skoufas, Konstantina Maragkopoulou, Antigone Tsiafitsa, Irini Sotiropoulou, Michalis Tsolakos, Effie Argyri, Mary Nikolaou, Eleni-Anna Vampouli, Christina Filippou, Katerina Gatsiou, Efstratios Dimitriadis, Tiina Laatikainen, Katja Wikström, Jemina Kivelä, Päivi Valve, Esko Levälahti, Eeva Virtanen, Vicky Van Stappen, Nele Huys, Ruben Willems, Samyah Shadid, Ivonne Panchyrz, Maxi Holland, Patrick Timpel, Stavros Liatis, George Dafoulas, Christina-Paulina Lambrinou, Angeliki Giannopoulou, Lydia Tsirigoti, Evi Fappa, Costas Anastasiou, Konstantina Zachari, Lala Rabemananjara, Maria Stella de Sabata, Winne Ko, Luis Moreno, Fernando Civeira, Gloria Bueno, Pilar De Miguel-Etayo, Esther Mª Gonzalez-Gil, Maria I Mesana, Germán Vicente-Rodriguez, Gerardo Rodriguez, Lucia Baila-Rueda, Ana Cenarro, Estíbaliz Jarauta, Rocío Mateo-Gallego, Violeta Iotova, Tsvetalina Tankova, Natalia Usheva, Kaloyan Tsochev, Nevena Chakarova, Sonya Galcheva, Rumyana Dimova, Yana Bocheva, Zhaneta Radkova, Vanya Marinova, Yuliya Bazdarska, Tanya Stefanova, Imre Rurik, Timea Ungvari, Zoltán Jancsó, Anna Nánási, László Kolozsvári, Csilla Semánova, Remberto Martinez, Marcos Tong, Kaisla Joutsenniemi, Katrina Wendel-Mitoraj, Yannis Manios, Christina Mavrogianni, Christina-Paulina Lambrinou, Greet Cardon, Jaana Lindström, Violeta Iotova, Tsvetalina Tankova, Fernando Civeira, Jemina Kivelä, Zoltán Jancsó, Samyah Shadid, Kaloyan Tsochev, Rocío Mateo-Gallego, Sándorné Radó, George Dafoulas, Konstantinos Makrilakis, Odysseas Androutsos, Feel4Diabetes-study group, Yannis Manios, Greet Cardon, Jaana Lindström, Peter Schwarz, Konstantinos Makrilakis, Lieven Annemans, Ignacio Garamendi, Meropi Kontogianni, Odysseas Androutsos, Christina Mavrogianni, Konstantina Tsoutsoulopoulou, Christina Katsarou, Eva Karaglani, Irini Qira, Efstathios Skoufas, Konstantina Maragkopoulou, Antigone Tsiafitsa, Irini Sotiropoulou, Michalis Tsolakos, Effie Argyri, Mary Nikolaou, Eleni-Anna Vampouli, Christina Filippou, Katerina Gatsiou, Efstratios Dimitriadis, Tiina Laatikainen, Katja Wikström, Jemina Kivelä, Päivi Valve, Esko Levälahti, Eeva Virtanen, Vicky Van Stappen, Nele Huys, Ruben Willems, Samyah Shadid, Ivonne Panchyrz, Maxi Holland, Patrick Timpel, Stavros Liatis, George Dafoulas, Christina-Paulina Lambrinou, Angeliki Giannopoulou, Lydia Tsirigoti, Evi Fappa, Costas Anastasiou, Konstantina Zachari, Lala Rabemananjara, Maria Stella de Sabata, Winne Ko, Luis Moreno, Fernando Civeira, Gloria Bueno, Pilar De Miguel-Etayo, Esther Mª Gonzalez-Gil, Maria I Mesana, Germán Vicente-Rodriguez, Gerardo Rodriguez, Lucia Baila-Rueda, Ana Cenarro, Estíbaliz Jarauta, Rocío Mateo-Gallego, Violeta Iotova, Tsvetalina Tankova, Natalia Usheva, Kaloyan Tsochev, Nevena Chakarova, Sonya Galcheva, Rumyana Dimova, Yana Bocheva, Zhaneta Radkova, Vanya Marinova, Yuliya Bazdarska, Tanya Stefanova, Imre Rurik, Timea Ungvari, Zoltán Jancsó, Anna Nánási, László Kolozsvári, Csilla Semánova, Remberto Martinez, Marcos Tong, Kaisla Joutsenniemi, Katrina Wendel-Mitoraj

Abstract

Background: The implementation of population screening and early prevention strategies targeting individuals at high-risk for type 2 diabetes (T2D) seems to be a public health priority. The current work aimed to describe the screening procedure applied in the Feel4Diabetes-study and examine its effectiveness in identifying individuals and families at high risk, primarily for T2D and secondarily for hypertension, among vulnerable populations in low to middle-income countries (LMICs) and high-income countries (HICs) across Europe.

Methods: A two-stage screening procedure, using primary schools as the entry-point to the community, was applied in low socioeconomic status (SES) regions in LMICs (Bulgaria-Hungary), HICs (Belgium-Finland) and HICs under austerity measures (Greece-Spain). During the first-stage screening via the school-setting, a total of 20,501 parents (mothers and/or fathers) of schoolchildren from 11,396 families completed the Finnish Diabetes Risk Score (FINDRISC) questionnaire, while their children underwent anthropometric measurements in the school setting. Parents from the identified "high-risk families" (n = 4484) were invited to participate in the second-stage screening, including the measurement of fasting plasma glucose (FPG) and blood pressure (BP). In total, 3153 parents participated in the second-stage screening (mean age 41.1 ± 5.6 years, 65.8% females).

Results: Among parents who attended the second-stage screening, the prevalence of prediabetes (as defined by impaired fasting glucose; FPG 100-125 mg/dl) and T2D (FPG > 126 mg/dl) was 23.2 and 3.0% respectively, and it was found to be higher in the higher FINDRISC categories. The percentage of undiagnosed T2D among the participants identified with T2D was 53.5%. The prevalence of high normal BP (systolic BP 130-139 mmHg and/ or diastolic BP 85-89 mmHg) and hypertension (systolic BP ≥ 140 mmHg and/ or diastolic BP ≥ 90 mmHg) was 14 and 18.6% respectively, which was also higher in the higher FINDRISC categories. The percentage of cases not receiving antihypertensive treatment among the participants identified with hypertension was 80.3%.

Conclusion: The findings of the current study indicate that the two-stage school and community-based screening procedure followed, effectively identified high-risk individuals and families in vulnerable populations across Europe. This approach could be potentially scalable and sustainable and support initiatives for the early prevention of T2D and hypertension.

Trial registration: The Feel4Diabetes-intervention is registered at https://ichgcp.net/clinical-trials-registry/NCT02393872" title="See in ClinicalTrials.gov">NCT02393872; date of trial registration: March 20, 2015).

Keywords: Hypertension; School-based; Screening; Type 2 diabetes; Vulnerable groups.

Conflict of interest statement

OA is a member of the Editorial Board of BMC Endocrine Disorders. He also acted as Guest Editor in the current Supplement Issue. None of the rest of the authors has any conflict to declare.

Figures

Fig. 1
Fig. 1
Prevalence of prediabetes and diabetes in parents participated in the second-stage screening by FINDRISC category. P-values indicate the significance of the differences among FINDRISC categories: 0–11 (low and slightly elevated risk), 12–14 (moderate risk), 15–16 (high and very high risk). Figures sharing the same superscript letters differentiate significantly from each other. FINDRISC: Finnish Diabetes Risk Score; HICs: High-income countries; LMICs: Low to middle-income countries
Fig. 2
Fig. 2
Prevalence of high normal blood pressure and hypertension in parents participated in the second-stage screening by FINDRISC category. P-values indicate the significance of the differences among FINDRISC categories: 0–11 (low and slightly elevated risk), 12–14 (moderate risk), 15–16 (high and very high risk). Figures sharing the same superscript letters differentiate significantly from each other. FINDRISC: Finnish Diabetes Risk Score; HICs: High-income countries; LMICs: Low to middle-income countries

References

    1. International Diabetes Federation (IDF) Diabetes Atlas 8th Edition (2017). Accessed 18 Oct 2019.
    1. Global Burden of Metabolic Risk Factors for Chronic Diseases Collaboration Cardiovascular disease, chronic kidney disease, and diabetes mortality burden of cardiometabolic risk factors from 1980 to 2010: a comparative risk assessment. Lancet Diabetes Endocrinol. 2014;2(8):634–647. doi: 10.1016/S2213-8587(14)70102-0.
    1. Agardh E, Allebeck P, Hallqvist J, Moradi T, Sidorchuk A. Type 2 diabetes incidence and socio-economic position: a systematic review and meta-analysis. Int J Epidemiol. 2011;40(3):804–818.
    1. Bilal U, Auchincloss AH, Diez-Roux AV. Neighborhood environments and diabetes risk and control. Curr Diabetes Rep. 2018;18(9):62. doi: 10.1007/s11892-018-1032-2.
    1. Sacerdote C, Ricceri F, Rolandsson O, Baldi I, Chirlaque MD, Feskens E, et al. Lower educational level is a predictor of incident type 2 diabetes in European countries: the EPIC-InterAct study. Int J Epidemiol. 2012;41(4):1162–1173. doi: 10.1093/ije/dys091.
    1. Tuomilehto J, Lindstrom J, Eriksson JG, Valle TT, Hamalainen H, Ilanne-Parikka P, et al. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med. 2001;344(18):1343–1350.
    1. Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA, et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med. 2002;346(6):393–403.
    1. Herman WH, Ye W, Griffin SJ, Simmons RK, Davies MJ, Khunti K, et al. Early detection and treatment of type 2 diabetes reduce cardiovascular morbidity and mortality: a simulation of the results of the Anglo-Danish-Dutch study of intensive treatment in people with screen-detected diabetes in primary care (ADDITION-Europe) Diabetes Care. 2015;38(8):1449–1455. doi: 10.2337/dc14-2459.
    1. Simmons RK, Griffin SJ, Lauritzen T, Sandbaek A. Effect of screening for type 2 diabetes on risk of cardiovascular disease and mortality: a controlled trial among 139,075 individuals diagnosed with diabetes in Denmark between 2001 and 2009. Diabetologia. 2017;60(11):2192–2199. doi: 10.1007/s00125-017-4299-y.
    1. Craigie AM, Lake AA, Kelly SA, Adamson AJ, Mathers JC. Tracking of obesity-related behaviours from childhood to adulthood: a systematic review. Maturitas. 2011;70(3):266–284. doi: 10.1016/j.maturitas.2011.08.005.
    1. Lloyd LJ, Langley-Evans SC, McMullen S. Childhood obesity and risk of the adult metabolic syndrome: a systematic review. Int J Obes (2005) 2012;36(1):1–11. doi: 10.1038/ijo.2011.186.
    1. Golan M. Parents as agents of change in childhood obesity from research to practice. Int Pediatr Obes. 2006;1(2):66–76. doi: 10.1080/17477160600644272.
    1. Baig AA, Benitez A, Quinn MT, Burnet DL. Family interventions to improve diabetes outcomes for adults. Ann N Y Acad Sci. 2015;1353:89–112. doi: 10.1111/nyas.12844.
    1. Khunti K, Gillies CL, Taub NA, Mostafa SA, Hiles SL, Abrams KR, et al. A comparison of cost per case detected of screening strategies for type 2 diabetes and impaired glucose regulation: modelling study. Diabetes Res Clin Pract. 2012;97(3):505–513. doi: 10.1016/j.diabres.2012.03.009.
    1. Khunti K, Mani H, Achana F, Cooper N, Gray LJ, Davies MJ. Systematic review and meta-analysis of response rates and diagnostic yield of screening for type 2 diabetes and those at high risk of diabetes. PLoS One. 2015;10(9):e0135702. doi: 10.1371/journal.pone.0135702.
    1. International Diabetes Federation (IDF). Recommendations For Managing Type 2 Diabetes In Primary Care (2017) . Accessed 18 Oct 2019.
    1. Ryden L, Grant PJ, Anker SD, Berne C, Cosentino F, Danchin N, et al. ESC guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD: the task force on diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and developed in collaboration with the European Association for the Study of diabetes (EASD) Eur Heart J. 2013;34(39):3035–3087. doi: 10.1093/eurheartj/eht108.
    1. Lindstrom J, Tuomilehto J. The diabetes risk score: a practical tool to predict type 2 diabetes risk. Diabetes Care. 2003;26(3):725–731. doi: 10.2337/diacare.26.3.725.
    1. Sargeant LA, Simmons RK, Barling RS, Butler R, Williams KM, Prevost AT, et al. Who attends a UK diabetes screening programme? Findings from the ADDITION-Cambridge study. Diabetic Med. 2010;27(9):995–1003. doi: 10.1111/j.1464-5491.2010.03056.x.
    1. Tsimihodimos V, Gonzalez-Villalpando C, Meigs JB, Ferrannini E. Hypertension and Diabetes Mellitus: Coprediction and Time Trajectories. Hypertension (Dallas, Tex : 1979) 2018;71(3):422–428. doi: 10.1161/HYPERTENSIONAHA.117.10546.
    1. Manios Yannis, Androutsos Odysseas, Lambrinou Christina-Paulina, Cardon Greet, Lindstrom Jaana, Annemans Lieven, Mateo-Gallego Rocio, de Sabata Maria Stella, Iotova Violeta, Kivela Jemina, Martinez Remberto, Moreno Luis A, Rurik Imre, Schwarz Peter, Tankova Tsvetalina, Liatis Stavros, Makrilakis Konstantinos. A school- and community-based intervention to promote healthy lifestyle and prevent type 2 diabetes in vulnerable families across Europe: design and implementation of the Feel4Diabetes-study. Public Health Nutrition. 2018;21(17):3281–3290. doi: 10.1017/S1368980018002136.
    1. World Bank Group . World Development Indicators 2014. Washington, DC: World Bank Publications; 2014.
    1. Eurostat . Euro Area and EU28 Government Deficit at 0.9 and 1.0% of GDP Respectively. Luxembourg: Eurostat; 2018.
    1. NCD Risk Factor Collaboration (NCD-RisC) Worldwide trends in diabetes since 1980: a pooled analysis of 751 population-based studies with 4.4 million participants. Lancet (London, England) 2016;387(10027):1513–1530. doi: 10.1016/S0140-6736(16)00618-8.
    1. Hellenic Statistical Authority (ELSTAT) Accessed 18 Oct 2019.
    1. VDAB-Arvastat. . Accessed 18 Oct 2019.
    1. Statistics Finland's PxWeb databases . Accessed 18 Oct 2019.
    1. Instituto Aragonés de Estadística (IAEST) . Accessed 18 Oct 2019.
    1. Costas A, Fappa E, Zachari K, Mavrogianni C, Van Stappen V, Kivelä J, Virtanen E, González-Gil E, Flores Barrantes P, Nánási A, Semánová C, Dimova R, Usheva N, Iotova V, Greet C, Manios Y, Makrilakis K. Development and reliability of questionnaires for the assessment of diet and physical activity behaviors in a multi-country sample in Europe the Feel4Diabetes Study [paper published supplement].
    1. Androutsos O, Costas A, Lambrinou C-P, Mavrogianni C, Cardon G, Van Stappen V, Kivelä J, Wikström K, Moreno LA, Iotova V, Tsochev K, Chakarova N, Ungvári T, Jancso Z, Makrilakis K, Manios Y, on behalf of the Feel4diabetes-study group. Intra- and inter- observer reliability of anthropometric measurements and blood pressure in primary schoolchildren and adults. The Feel4Diabetes-study [paper published in the current supplement].
    1. . Assessed 18 Oct 2019.
    1. Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatric obesity. 2012;7(4):284–294. doi: 10.1111/j.2047-6310.2012.00064.x.
    1. American Diabetes Association 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2018. Diabetes Care. 2018;41(Suppl 1):S13–s27. doi: 10.2337/dc18-S002.
    1. Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, et al. 2018 ESC/ESH guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension: the task force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension. J Hypertens. 2018;36(10):1953–2041. doi: 10.1097/HJH.0000000000001940.
    1. WHO . Obesity: preventing and managing the global epidemic Report of a WHO Consultation. Geneva: WHO; 2000.
    1. Simmons D, Zgibor JC. Should we screen for type 2 diabetes among asymptomatic individuals? Yes. Diabetologia. 2017;60(11):2148–2152. doi: 10.1007/s00125-017-4397-x.
    1. Gagliardino JJ, Elgart JF. Diabetes primary prevention program: New insights from data analysis of recruitment period. Diabetes Metab Res Rev. 2018;34(1):e2943. doi: 10.1002/dmrr.2943.
    1. Cos FX, Barengo NC, Costa B, Mundet-Tuduri X, Lindstrom J, Tuomilehto JO. Screening for people with abnormal glucose metabolism in the European DE-PLAN project. Diabetes Res Clin Pract. 2015;109(1):149–156. doi: 10.1016/j.diabres.2015.04.016.
    1. Franciosi M, De Berardis G, Rossi MC, Sacco M, Belfiglio M, Pellegrini F, et al. Use of the diabetes risk score for opportunistic screening of undiagnosed diabetes and impaired glucose tolerance: the IGLOO (impaired glucose tolerance and long-term outcomes observational) study. Diabetes Care. 2005;28(5):1187–1194. doi: 10.2337/diacare.28.5.1187.
    1. Mavrogianni C, Lambrinou CP, Androutsos O, Lindstrom J, Kivela J, Cardon G, et al. Evaluation of the Finnish diabetes risk score as a screening tool for undiagnosed type 2 diabetes and dysglycaemia among early middle-aged adults in a large-scale European cohort. The Feel4Diabetes-study. Diabetes Res Clin Pract. 2019;150:99–110. doi: 10.1016/j.diabres.2019.02.017.
    1. Casagrande SS, Cowie CC, Genuth SM. Self-reported prevalence of diabetes screening in the U.S., 2005-2010. Am J Prev Med. 2014;47(6):780–787. doi: 10.1016/j.amepre.2014.07.039.
    1. Psaltopoulou T, Orfanos P, Naska A, Lenas D, Trichopoulos D, Trichopoulou A. Prevalence, awareness, treatment and control of hypertension in a general population sample of 26,913 adults in the Greek EPIC study. Int J Epidemiol. 2004;33(6):1345–1352. doi: 10.1093/ije/dyh249.
    1. Wagner A, Sadoun A, Dallongeville J, Ferrieres J, Amouyel P, Ruidavets JB, et al. High blood pressure prevalence and control in a middle-aged French population and their associated factors: the MONA LISA study. J Hypertens. 2011;29(1):43–50. doi: 10.1097/HJH.0b013e32833f9c4d.
    1. Tocci G, Nati G, Cricelli C, Parretti D, Lapi F, Ferrucci A, et al. Prevalence and control of hypertension in the general practice in Italy: updated analysis of a large database. J Hum Hypertens. 2017;31(4):258–262. doi: 10.1038/jhh.2016.71.
    1. Fizelova M, Jauhiainen R, Stancakova A, Kuusisto J, Laakso M. Finnish diabetes risk score is associated with impaired insulin secretion and insulin sensitivity, drug-treated hypertension and cardiovascular disease: a follow-up study of the METSIM cohort. PLoS One. 2016;11(11):e0166584. doi: 10.1371/journal.pone.0166584.
    1. Pereira M, Lunet N, Azevedo A, Barros H. Differences in prevalence, awareness, treatment and control of hypertension between developing and developed countries. J Hypertens. 2009;27(5):963–975. doi: 10.1097/HJH.0b013e3283282f65.
    1. Chow CK, Teo KK, Rangarajan S, Islam S, Gupta R, Avezum A, et al. Prevalence, awareness, treatment, and control of hypertension in rural and urban communities in high-, middle-, and low-income countries. Jama. 2013;310(9):959–968. doi: 10.1001/jama.2013.184182.
    1. Wang Y, Min J, Khuri J, Li M. A Systematic Examination of the Association between Parental and Child Obesity across Countries. Adv Nutr (Bethesda, Md) 2017;8(3):436–448. doi: 10.3945/an.116.013235.
    1. Ritchie LD, Welk G, Styne D, Gerstein DE, Crawford PB. Family environment and pediatric overweight: what is a parent to do? J Am Diet Assoc. 2005;105(5 Suppl 1):S70–S79. doi: 10.1016/j.jada.2005.02.017.

Source: PubMed

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