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      The association between diabetes mellitus and incident infections: a systematic review and meta-analysis of observational studies

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          Abstract

          Objective

          To quantify the association between diabetes and the risk of incident infections by conducting a systematic review and meta-analysis.

          Research design and methods

          Two reviewers independently screened articles identified from PubMed, EMBASE, Cochrane Library, IPA, and Web of Science databases. Cohort studies (CS) or case–control studies (CCS) evaluating the incidence of infections in adults with diabetes were included. Infections were classified as: skin and soft tissue, respiratory, blood, genitourinary, head and neck, gastrointestinal, bone, viral, and non-specified infections. Study quality was assessed using the Newcastle-Ottawa Quality Assessment Scale. Summary crude and adjusted OR with 95% CIs were calculated using random effects models, stratified by study design. Heterogeneity was measured using the I 2statistic and explored using subgroup analyses.

          Results

          A total of 345 (243 CS and 102 CCS) studies were included. Combining adjusted results from all CS, diabetes was associated with an increased incidence of skin (OR 1.94, 95% CI 1.78 to 2.12), respiratory (OR 1.35, 95% CI 1.28 to 1.43), blood (OR 1.72, 95% CI 1.48 to 2.00), genitourinary (OR 1.61, 95% CI 1.42 to 1.82), head and neck (OR 1.17, 95% CI 1.13 to 1.22), gastrointestinal (OR 1.48, 95% CI 1.40 to 1.57), viral (OR 1.29, 95% CI 1.13 to 1.46), and non-specified (OR 1.84, 95% CI 1.66 to 2.04) infections. A stronger association was observed among CCS: skin (OR 2.64, 95% CI 2.20 to 3.17), respiratory (OR 1.62, 95% CI 1.37 to 1.92), blood (OR 2.40, 95% CI 1.68 to 3.42), genitourinary (OR 2.59, 95% CI 1.60 to 4.17), gastrointestinal (OR 3.61, 95% CI 2.94 to 4.43), and non-specified (OR 3.53, 95% CI 2.62 to 4.75).

          Conclusion

          Diabetes is associated with an increased risk of multiple types of infections. A high degree of heterogeneity was observed; however, subgroup analysis decreased the amount of heterogeneity within most groups. Results were generally consistent across types of infections.

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          Most cited references42

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          Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure.

          Yuji Okura, Lynn H. Urban, Douglas Mahoney … (2004)
          Questionnaires are used to estimate disease burden. Agreement between questionnaire responses and a criterion standard is important for optimal disease prevalence estimates. We measured the agreement between self-reported disease and medical record diagnosis of disease. A total of 2,037 Olmsted County, Minnesota residents > or =45 years of age were randomly selected. Questionnaires asked if subjects had ever had heart failure, diabetes, hypertension, myocardial infarction (MI), or stroke. Medical records were abstracted. Self-report of disease showed >90% specificity for all these diseases, but sensitivity was low for heart failure (69%) and diabetes (66%). Agreement between self-report and medical record was substantial (kappa 0.71-0.80) for diabetes, hypertension, MI, and stroke but not for heart failure (kappa 0.46). Factors associated with high total agreement by multivariate analysis were age 12 years, and zero Charlson Index score (P < .05). Questionnaire data are of greatest value in life-threatening, acute-onset diseases (e.g., MI and stroke) and chronic disorders requiring ongoing management (e.g.,diabetes and hypertension). They are more accurate in young women and better-educated subjects.
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            Mortality and causes of death in the WHO Multinational Study of Vascular Disease in Diabetes.

            N. Morrish, S.-L. Wang, L Stevens … (2001)
            We aimed to examine the mortality rates, excess mortality and causes of death in diabetic patients from ten centres throughout the world. A mortality follow-up of 4713 WHO Multinational Study of Vascular Disease in Diabetes (WHO MSVDD) participants from ten centres was carried out, causes of death were ascertained and age-adjusted mortality rates were calculated by centre, sex and type of diabetes. Excess mortality, compared with the background population, was assessed in terms of standardised mortality ratios (SMRs) for each of the 10 cohorts. Cardiovascular disease was the most common underlying cause of death, accounting for 44 % of deaths in Type I (insulin-dependent) diabetes mellitus and 52 % of deaths in Type II (non-insulin-dependent) diabetes mellitus. Renal disease accounted for 21% of deaths in Type I diabetes and 11% in Type II diabetes. For Type I diabetes, all-cause mortality rates were highest in Berlin men and Warsaw women, and lowest in London men and Zagreb women. For Type II diabetes, rates were highest in Warsaw men and Oklahoma women and lowest in Tokyo men and women. Age adjusted mortality rates and SMRs were generally higher in patients with Type I diabetes compared with those with Type II diabetes. Men and women in the Tokyo cohort had a very low excess mortality when compared with the background population. This study confirms the importance of cardiovascular disease as the major cause of death in people with both types of diabetes. The low excess mortality in the Japanese cohort could have implications for the possible reduction of the burden of mortality associated with diabetes in other parts of the world.
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              Impaired leucocyte functions in diabetic patients.

              M Delamaire, D Maugendre, M. Moreno … (1997)
              This study evaluates polymorphonuclear neutrophil (PMN) cell performance in 61 diabetic patients free of infection (40 Type 1, 21 Type 2), using tests that explore all the functional steps of PMN: (1) adherence: expression of adhesion molecules, CD 11a, CD 11b, CD 11c; nylon fiber adherence test; (2) chemotaxis under agarose towards the bacterial oligopeptide FMLP and complement fractions, used as attracting agents; (3) phagocytosis of opsonized latex microbeads; (4) bactericidal activity: chemiluminescence assessment of the oxidative killing potential before and after stimulation by opsonized zymosan and PMA; nitroblue tetrazolium reduction test. Results were analysed according to potentially influential factors: metabolic control (HbA1C, glycaemia), age of patient, type of diabetes, disease duration, and existence of vascular complications. PMN chemotaxis was significantly lower in patients than in healthy controls (p < 0.001) and associated with spontaneous adherence and increased expression of adhesion molecules (CD 11b, CD 11c). The increased response to chemiluminescence reflects spontaneous activation of PMN cells and increased free radical production; after stimulation, response was lower than in controls. The type of diabetes, the age of patients, HbA1C level and disease duration did not affect the responses. Chemotaxis and chemiluminescence were further reduced in patients with vascular complications and hyperglycaemia. We conclude that all steps of PMN functioning are altered in diabetic patients, which may increase the risk of vascular complications and infectious episodes.
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                Author and article information

                Journal
                Journal ID (nlm-ta): BMJ Open Diabetes Res Care
                Journal ID (iso-abbrev): BMJ Open Diabetes Res Care
                Journal ID (hwp): bmjdrc
                Journal ID (publisher-id): bmjdrc
                Title: BMJ Open Diabetes Research & Care
                Publisher: BMJ Open Diabetes Research & Care (BMA House, Tavistock Square, London, WC1H 9JR )
                ISSN (Electronic): 2052-4897
                Publication date Collection: 2017
                Publication date (Electronic): 27 May 2017
                Volume: 5
                Issue: 1
                Electronic Location Identifier: e000336
                Affiliations
                [1 ] departmentSchool of Pharmacy , Memorial University of Newfoundland , St. John’s, Newfoundland and Labrador, Canada
                [2 ] departmentFaculty of Medicine , Memorial University of Newfoundland , St. John’s, Newfoundland and Labrador, Canada
                Author notes
                [Correspondence to ] Dr John-Michael Gamble; jgamble@ 123456mun.ca
                Author information
                http://orcid.org/0000-0001-6891-8721
                Article
                Publisher ID: bmjdrc-2016-000336
                DOI: 10.1136/bmjdrc-2016-000336
                PMC ID: 5530269
                SO-VID: 727acb66-bdd2-440b-a56c-5b9191011fa2
                Copyright © © Article author(s) (or their employer(s) unless otherwise stated in the text of the article) 2017. All rights reserved. No commercial use is permitted unless otherwise expressly granted.
                License:

                This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/

                History
                Date received : 30 September 2016
                Date revision received : 03 February 2017
                Date accepted : 21 March 2017
                Categories
                Subject: Epidemiology/Health Services Research
                Subject: 1506
                Subject: 1867
                Custom metadata
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                Keywords: diabetes,infection,observational studies,systematic review,meta-analysis.
                Data availability:
                Keywords: diabetes, infection, observational studies, systematic review, meta-analysis.

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