Staphylococcus aureus and Pseudomonas aeruginosa co-infection is associated with cystic fibrosis-related diabetes and poor clinical outcomes

European Journal of Clinical Microbiology and Infectious Diseases

Volumn 35, Issue 6, 2016, Pages 947-953

  Limoli, D H ^a,b   Yang, J ^c   Khansaheb, M K ^a   Helfman, B ^a,b   Peng, L ^c   Stecenko, A A ^a,b   Goldberg, J B ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Emory + Children's Center for CF and Airways Disease Research   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GLUCOSE; HEMOGLOBIN A1C;

ADULT; ARTICLE; CYSTIC FIBROSIS; CYSTIC FIBROSIS RELATED DIABETES; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE EXACERBATION; FEMALE; FORCED EXPIRATORY VOLUME; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; GLYCEMIC CONTROL; HUMAN; IMPAIRED GLUCOSE TOLERANCE; LUNG FUNCTION; MAJOR CLINICAL STUDY; MALE; MICROBIAL COMMUNITY; MIXED INFECTION; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RESPIRATORY TRACT INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ADOLESCENT; CHILD; COMPLICATION; GENETICS; GEORGIA; HEALTH SURVEY; ODDS RATIO; PSEUDOMONAS INFECTIONS; REGISTER; STAPHYLOCOCCAL INFECTIONS; YOUNG ADULT;

ADOLESCENT; ADULT; CHILD; COINFECTION; CYSTIC FIBROSIS; DIABETES MELLITUS; FEMALE; GEORGIA; HUMANS; MALE; ODDS RATIO; PATIENT OUTCOME ASSESSMENT; POPULATION SURVEILLANCE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; REGISTRIES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; YOUNG ADULT;

EID: 84961200401     PISSN: 09349723     EISSN: 14354373     Source Type: Journal    
DOI: 10.1007/s10096-016-2621-0     Document Type: Article

References (28)

1. Ciofu O, Tolker-Nielsen T, Jensen PØ, Wang H, Høiby N (2015) Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Adv Drug Deliv Rev 85:7–23. doi:10.1016/j.addr.2014.11.017
2. O’Sullivan BP, Freedman SD (2009) Cystic fibrosis. Lancet 373:1891–1904
3. Lek N, Acerini CL (2010) Cystic fibrosis related diabetes mellitus—diagnostic and management challenges. Curr Diabetes Rev 6(1):9–16. doi:10.2174/157339910790442600
4. Finkelstein SM, Wielinski CL, Elliott GR, Warwick WJ, Barbosa J, Wu SC et al (1988) Diabetes mellitus associated with cystic fibrosis. J Pediatr 112:373–377
5. Koch C, Rainisio M, Madessani U, Harms HK, Hodson ME, Mastella G et al (2001) Presence of cystic fibrosis-related diabetes mellitus is tightly linked to poor lung function in patients with cystic fibrosis: data from the European Epidemiologic Registry of Cystic Fibrosis. Pediatr Pulmonol 32:343–350. doi:10.1002/ppul.1142
6. Marshall BC, Butler SM, Stoddard M, Moran AM, Liou TG, Morgan WJ (2005) Epidemiology of cystic fibrosis-related diabetes. J Pediatr 146:681–687. doi:10.1016/j.jpeds.2004.12.039
7. Milla CE, Warwick WJ, Moran A (2000) Trends in pulmonary function in patients with cystic fibrosis correlate with the degree of glucose intolerance at baseline. Am J Respir Crit Care Med 162:891–895
8. Kerem E, Viviani L, Zolin A, MacNeill S, Hatziagorou E, Ellemunter H et al (2014) Factors associated with FEV1 decline in cystic fibrosis: analysis of the ECFS patient registry. Eur Respir J 43:125–133
9. Parkins MD, Rendall JC, Elborn JS (2012) Incidence and risk factors for pulmonary exacerbation treatment failures in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa. Chest 141:485–493. doi:10.1378/chest.11-0917
10. Lanng S, Thorsteinsson B, Nerup J, Koch C (1994) Diabetes mellitus in cystic fibrosis: effect of insulin therapy on lung function and infections. Acta Paediatr 83:849–853
11. Merlo CA, Boyle MP, Diener-West M, Marshall BC, Goss CH, Lechtzin N (2007) Incidence and risk factors for multiple antibiotic-resistant Pseudomonas aeruginosa in cystic fibrosis. Chest 132:562–568. doi:10.1378/chest.06-2888
12. Klepac-Ceraj V, Lemon KP, Martin TR, Allgaier M, Kembel SW, Knapp AA et al (2010) Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environ Microbiol 12:1293–1303. doi:10.1111/j.1462-2920.2010.02173.x
13. McGuigan L, Callaghan M (2015) The evolving dynamics of the microbial community in the cystic fibrosis lung. Environ Microbiol 17:16–28. doi:10.1111/1462-2920.12504
14. Paganin P, Fiscarelli EV, Tuccio V, Chiancianesi M, Bacci G, Morelli P et al (2015) Changes in cystic fibrosis airway microbial community associated with a severe decline in lung function. PLoS One 10:e0124348. doi:10.1371/journal.pone.0124348
15. American Diabetes Association (2015) Classification and diagnosis of diabetes. Diabetes Care 38(Suppl):S8–S16. doi:10.2337/dc15-S005
16. Knudson RJ, Lebowitz MD, Holberg CJ, Burrows B (1983) Changes in the normal maximal expiratory flow-volume curve with growth and aging. Am Rev Respir Dis 127(6):725–734
17. Moran A, Brunzell C, Cohen RC, Katz M, Marshall BC, Onady G et al (2010) Clinical care guidelines for cystic fibrosis-related diabetes. Diabetes Care 33:2697–2708
18. Hubert D, Réglier-Poupet H, Sermet-Gaudelus I, Ferroni A, Le Bourgeois M, Burgel P-R et al (2013) Association between Staphylococcus aureus alone or combined with Pseudomonas aeruginosa and the clinical condition of patients with cystic fibrosis. J Cyst Fibros 12:497–503. doi:10.1016/j.jcf.2012.12.003
19. Brennan AL, Gyi KM, Wood DM, Johnson J, Holliman R, Baines DL et al (2007) Airway glucose concentrations and effect on growth of respiratory pathogens in cystic fibrosis. J Cyst Fibros 6:101–109. doi:10.1016/j.jcf.2006.03.009
20. Wood DM, Brennan AL, Philips BJ, Baker EH (2004) Effect of hyperglycaemia on glucose concentration of human nasal secretions. Clin Sci (Lond) 106:527–533. doi:10.1042/CS20030333
21. Baker EH, Clark N, Brennan AL, Fisher DA, Gyi KM, Hodson ME et al (2007) Hyperglycemia and cystic fibrosis alter respiratory fluid glucose concentrations estimated by breath condensate analysis. J Appl Physiol (1985) 102:1969–1975. doi:10.1152/japplphysiol.01425.2006
22. Garnett JP, Nguyen TT, Moffatt JD, Pelham ER, Kalsi KK, Baker EH et al (2012) Proinflammatory mediators disrupt glucose homeostasis in airway surface liquid. J Immunol 189:373–380. doi:10.4049/jimmunol.1200718
23. Philips BJ, Redman J, Brennan A, Wood D, Holliman R, Baines D et al (2005) Glucose in bronchial aspirates increases the risk of respiratory MRSA in intubated patients. Thorax [Internet] 60:761–764
24. Baker EH, Janaway CH, Philips BJ, Brennan AL, Baines DL, Wood DM et al (2006) Hyperglycaemia is associated with poor outcomes in patients admitted to hospital with acute exacerbations of chronic obstructive pulmonary disease. Thorax 61:284–289. doi:10.1136/thx.2005.051029
25. Alba-Loureiro TC, Munhoz CD, Martins JO, Cerchiaro GA, Scavone C, Curi R et al (2007) Neutrophil function and metabolism in individuals with diabetes mellitus. Braz J Med Biol Res 40:1037–1044. doi:10.1590/S0100-879X2006005000143
26. Yano H, Kinoshita M, Fujino K, Nakashima M, Yamamoto Y, Miyazaki H et al (2012) Insulin treatment directly restores neutrophil phagocytosis and bactericidal activity in diabetic mice and thereby improves surgical site Staphylococcus aureus infection. Infect Immun 80(12):4409–4416. doi:10.1128/IAI.00787-12
27. Hunt WR, Zughaier SM, Guentert DE, Shenep MA, Koval M, McCarty NA et al (2014) Hyperglycemia impedes lung bacterial clearance in a murine model of cystic fibrosis-related diabetes. Am J Physiol Lung Cell Mol Physiol 306(1):L43–L49. doi:10.1152/ajplung.00224.2013
28. Mulrennan S, Baltic S, Aggarwal S, Wood J, Miranda A, Frost F et al (2015) The role of receptor for advanced glycation end products in airway inflammation in CF and CF related diabetes. Sci Rep 5:8931. doi:10.1038/srep08931