Opportunistic respiratory pathogens in the oral cavity of the elderly
Akio Tada
Department of Oral Health, National Institute of Public Health, Wako, Saitama, Japan
Search for more papers by this authorNobuhiro Hanada
Department of Translational Research, Tsurumi University, School of Dental Medicine, Tsurumi-ku, Yokohama, Japan
Search for more papers by this authorAkio Tada
Department of Oral Health, National Institute of Public Health, Wako, Saitama, Japan
Search for more papers by this authorNobuhiro Hanada
Department of Translational Research, Tsurumi University, School of Dental Medicine, Tsurumi-ku, Yokohama, Japan
Search for more papers by this authorEditor: Willem van Leeuwen
Abstract
The oral cavity of the hospitalized or bedridden elderly is often a reservoir for opportunistic pathogens associated with respiratory diseases. Commensal flora and the host interact in a balanced fashion and oral infections are considered to appear following an imbalance in the oral resident microbiota, leading to the emergence of potentially pathogenic bacteria. The definition of the process involved in colonization by opportunistic respiratory pathogens needs to elucidate the factors responsible for the transition of the microbiota from commensal to pathogenic flora. The regulatory factors influencing the oral ecosystem can be divided into three major categories: the host defense system, commensal bacteria, and external pathogens. In this article, we review the profile of these categories including the intricate cellular interaction between immune factors and commensal bacteria and the disturbance in homeostasis in the oral cavity of hospitalized or bedridden elderly, which facilitates oral colonization by opportunistic respiratory pathogens.
References
- Adachi M, Ishihara K, Abe S & Okuda K (2007) Professional oral health care by dental hygienists reduced respiratory infections in elderly persons requiring nursing care. Int J Dent Hyg 5: 69–74.
- Adair CG, Gorman SP, Feron BM et al. (1999) Implication of endotracheal tube biofilm for ventilator-associated pneumonia. Intens Care Med 25: 1072–1076.
- Adamsson I, Edlund C, Sjöstedt S & Nord CE (1997) Comparative effects of cefadroxil and phenoxymethylpenicillin on the normal oropharyngeal and intestinal microflora. Infection 25: 154–158.
- Adamsson I, Nord CE, Lundquist P, Sjöstedt S & Edlund C (1999) Comparative effects of omeprazole, amoxycillin plus metronidazole versus omeprazole, clarithromycin plus metronidazole on the oral, gastric and intestinal microflora in Helicobacter pylori-infected patients. J Antimicrob Chemoth 44: 629–640.
- Akimoto T, Kumai Y, Akama T, Hayashi E, Murakami H, Soma R, Kuno S & Kono I (2003) Effects of 12 months of exercise training on salivary secretory IgA levels in elderly subjects. Brit J Sport Med 37: 76–79.
- Al-Ahmad A, Wunder A, Auschill TM, Follo M, Braun G, Hellwig E & Arweiler NB (2007) The in vivo dynamics of Streptococcus spp., Actinomyces naeslundii, Fusobacterium nucleatum and Veillonella spp. in dental plaque biofilm as analysed by five-colour multiplex fluorescence in situ hybridization. J Med Microbiol 56: 681–687.
- Almirall J, Cabré M & Clavé P (2007) The incidence of aspiration pneumonia as determined according to swallowing function testing was high in CAP and hospital-acquired pneumonia. Aspiration pneumonia. A comprehensive review on aspiration pneumonia. Med Clin-Barcelona 129: 424–432.
- Almståhl A & Wikström M (1999) Oral microflora in subjects with reduced salivary secretion. J Dent Res 78: 1410–1416.
- Amerongen AV & Veerman EC (2002) Saliva – the defender of the oral cavity. Oral Dis 8: 12–22.
- Baba N, Samson S, Bourdet-Sicard R, Rubio M & Sarfati M (2008) Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells. J Leukocyte Biol 84: 468–476.
- Bergmans DC, Bonten MJ, Gaillard CA, Paling JC, Van Der Geest S, Van Tiel FH, Beysens AJ, De Leeuw PW & Stobberingh EE (2001) Prevention of ventilator-associated pneumonia by oral decontamination: a prospective, randomized, double-blind, placebo-controlled study. Am J Resp Crit Care 164: 382–388.
- Berry JA, Biedlingmaier JF & Whelan PJ (2000) In vitro resistance to bacterial biofilm formation on coated fluoroplastic tympanostomy tubes. Otolaryng Head Neck 123: 246–251.
- Biesbrock AR, Reddy MS & Levine MJ (1991) Interaction of a salivary mucin-secretory immunoglobulin A complex with mucosal pathogens. Infect Immun 59: 3492–3497.
- Blaise RB & Alexander RH (2008) agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 25: e1000052.
- Blandizzi C, Malizia T, Lupetti A, Pesce D, Gabriele M, Giuca MR, Campa M, Del Tacca M & Senesi S (1999) Periodontal tissue disposition of azithromycin in patients affected by chronic inflammatory periodontal diseases. J Periodontol 70: 960–966.
- Boirivant M & Strober W (2007) The mechanism of action of probiotics. Curr Opin Gastroen 23: 679–692.
- Bourdiol P, Mioche L & Monier S (2004) Effect of age on salivary flow obtained under feeding and non-feeding conditions. J Oral Rehabil 31: 445–452.
- Bowden GH & Hamilton IR (1987) Environmental pH as a factor in the competition between strains of oral streptococci, Streptococcus mutans, S. sanguis, and ‘S. mitior’ growing in continuous culture. Can J Microbiol 33: 824–827.
- Bowden GH & Hamilton IR (1998) Survival of oral bacteria. Crit Rev Oral Biol M 9: 54–85.
- Bradshaw DJ, Marsh PD, Allison C & Schilling KM (1996) Effect of oxygen, inoculum composition and flow rate on development of mixed-culture oral biofilms. Microbiology 142: 623–629.
- Burton JP, Wescombe PA, Moore CJ, Chilcott CN & Tagg JR (2006) Safety assessment of the oral cavity probiotic Streptococcus salivarius K12. Appl Environ Microb 72: 3050–3053.
- Busarcevic M, Kojic M, Dalgalarrondo M, Chobert JM, Haertlé T & Topisirovic L (2008) Purification of bacteriocin LS1 produced by human oral isolate Lactobacillus salivarius BGHO1. Oral Microbiol Immun 23: 254–258.
- Carlsson J (1997) Bacterial metabolism in dental biofilms. Adv Dent Res 11: 75–80.
- Chávez de Paz LE, Hamilton IR & Svensäter G (2008) Oral bacteria in biofilms exhibit slow reactivation from nutrient deprivation. Microbiology 154: 1927–1938.
- Chiu B (1999) Multiple infections in carotid atherosclerotic plaques. Am Heart J 138 (suppl 5 Pt 2): S534–S536.
- Chung WO & Dale BA (2004) Innate immune response of oral and foreskin keratinocytes: utilization of different signaling pathways by various bacterial species. Infect Immun 72: 352–358.
- Coleman P & Watson NM (2006) Oral care provided by certified nursing assistants in nursing homes. J Am Geriatr Soc 54: 138–143.
- Collier-Hyams LS & Neish AS (2005) Innate immune relationship between commensal flora and the mammalian intestinal epithelium. Cell Mol Life Sci 62: 1339–1348.
- Collier-Hyams LS, Sloane V, Batten BC & Neish AS (2005) Cutting edge: bacterial modulation of epithelial signaling via changes in neddylation of cullin-1. J Immunol 175: 4194–4198.
- Cosseau C, Devine DA, Dullaghan E et al. (2008) The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host–microbe homeostasis. Infect Immun 76: 4163–4175.
- Cunha BA (2005) Methicillin-resistant Staphylococcus aureus: clinical manifestations and antimicrobial therapy. Clin Microbiol Infec 11 (suppl 4): 33–42.
- Dale BA & Fredericks LP (2005) Antimicrobial peptides in the oral environment: expression and function in health and disease. Curr Issues Mol Biol 7: 119–133.
- Da Mata A, Da Silva Marques D, Silveira J, Marques J, De Melo Campos Felino E & Guilherme N (2009) Effects of gustatory stimulants of salivary secretion on salivary pH and flow: a randomized controlled trial. Oral Dis 15: 220–228.
- Daniel JH, Mark DS, Michael JS, Andrew BH, Charless CC & Joseph OM (2009) Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol 17: 130–138.
- Dawes C (2004) Factors influencing salivary flow rate and composition. Saliva and Oral Health, 3rd edn ( M Edgar, C Dawes & D O'Mullane, eds), pp. 32–49. British Dental Association, London.
- Dawes C (2008) Salivary flow patterns and the health of hard and soft oral tissues. J Am Dent Assoc 139 (suppl): 18S–24S.
- Dawes C & Kubieniec K (2004) The effects of prolonged gum chewing on salivary flow rate and composition. Arch Oral Biol 49: 665–669.
- Delcenserie V, Martel D, Lamoureux M, Amiot J, Boutin Y & Roy D (2008) Immunomodulatory effects of probiotics in the intestinal tract. Curr Issues Mol Biol 10: 37–54.
- Dennesen P, Van Der Ven A, Vlasveld M, Lokker L, Ramsay G, Kessels A, Van Den Keijbus P, Van Nieuw Amerongen A & Veerman E (2003) Inadequate salivary flow and poor oral mucosal status in intubated intensive care unit patients. Crit Care Med 31: 781–786.
- DeRiso AJ II, Ladowski JS, Dillon TA, Justice JW & Peterson AC (1996) Chlorhexidine gluconate 0.12% oral rinse reduces the incidence of total nosocomial respiratory infection and nonprophylactic systemic antibiotic use in patients undergoing heart surgery. Chest 109: 1556–1561.
- De Smet K & Contreras R (2005) Human antimicrobial peptides: defensins, cathelicidins and histatins. Biotechnol Lett 27: 1337–1347.
- De Souza Gonçalves L, Souto R & Colombo AP (2009) Detection of Helicobacter pylori, Enterococcus faecalis, and Pseudomonas aeruginosa in the subgingival biofilm of HIV-infected subjects undergoing HAART with chronic periodontitis. Eur J Clin Microbiol 28: 1135–1142.
- Devine DA (2003) Antimicrobial peptides in defence of the oral and respiratory tracts. Mol Immunol 40: 431–443.
- De Visschere LM, Grooten L, Theuniers G & Vanobbergen JN (2006) Oral hygiene of elderly people in long-term care institutions – a cross-sectional study. Gerodontology 23: 195–204.
- Diamond G, Beckloff N & Ryan LK (2008) Host defense peptides in the oral cavity and the lung: similarities and differences. J Dent Res 87: 915–927.
- Didilescu AC, Skaug N, Marica C & Didilescu C (2005) Respiratory pathogens in dental plaque of hospitalized patients with chronic lung diseases. Clin Oral Invest 9: 141–147.
- Dormenval V, Budtz-Jørgensen E, Mojon P, Bruyère A & Rapin CH (1998) Associations between malnutrition, poor general health and oral dryness in hospitalized elderly patients. Age Ageing 27: 123–128.
- Ducci M, Scalori V, Del Tacca M, Soldami G, Bernardini C, Grothe E & Bertelli A (1981) The pharmacokinetics of two erythromycin esters in plasma and in saliva following oral administration in humans. Int J Clin Pharm Th Toxicol 19: 494–497.
- Edlund C, Alván G, Barkholt L, Vacheron F & Nord CE (2000) Pharmacokinetics and comparative effects of telithromycin (HMR 3647) and clarithromycin on the oropharyngeal and intestinal microflora. J Antimicrob Chemoth 46: 741–749.
- El-Solh AA, Pietrantoni C, Bhat A, Okada M, Zambon J, Aquilina A & Berbary E (2004) Colonization of dental plaques: a reservoir of respiratory pathogens for hospital-acquired pneumonia in institutionalized elders. Chest 126: 1575–1582.
- Estes RJ & Meduri GU (1995) The pathogenesis of ventilator-associated pneumonia: I. Mechanisms of bacterial transcolonization and airway inoculation. Intens Care Med 21: 365–383.
- Fanello S, Bouchara JP, Jousset N, Delbos V & LeFlohic AM (2001) Nosocomial Candida albicans acquisition in a geriatric unit: epidemiology and evidence for person-to-person transmission. J Hosp Infect 47: 46–52.
- Fanello S, Bouchara JP, Sauteron M, Delbos V, Parot E, Marot-Leblond A, Moalic E, Le Flohicc AM & Brangerd B (2006) Predictive value of oral colonization by Candida yeasts for the onset of a nosocomial infection in elderly hospitalized patients. J Med Microbiol 55: 223–228.
- Favre-Bonté S, Chamot E, Köhler T, Romand JA & Van Delden C (2007) Autoinducer production and quorum-sensing dependent phenotypes of Pseudomonas aeruginosa vary according to isolation site during colonization of intubated patients. BMC Microbiol 7: 33.
- Fourrier F, Duvivier B, Boutigny H, Roussel-Delvallez M & Chopin C (1998) Colonization of dental plaque: a source of nosocomial infections in intensive care unit patients. Crit Care Med 26: 301–308.
- Fourrier F, Cau-Pottier E, Boutigny H, Roussel-Delvallez M, Jourdain M & Chopin C (2000) Effects of dental plaque antiseptic decontamination on bacterial colonization and nosocomial infections in critically ill patients. Intens Care Med 26: 1239–1247.
- Frenkel H, Harvey I & Newcombe RG (2001) Improving oral health in institutionalized elderly people by educating caregivers: a randomized controlled trial. Community Dent Oral 29: 289–297.
- Frenkel H, Harvey I & Needs K (2002) ‘Oral health care education and its effect on caregivers’ knowledge and attitudes: a randomized controlled trial. Community Dent Oral 30: 91–100.
- Fujiwara D, Wei B, Presley LL, Brewer S, McPherson M, Lewinski MA, Borneman J & Braun J (2008) Systemic control of plasmacytoid dendritic cells by CD8+ T cells and commensal microbiota. J Immunol 180: 5843–5852.
- Fure S & Zickert I (1990) Salivary conditions and cariogenic microorganisms in 55, 65, and 75-year-old Swedish subjects. Scand J Dent Res 98: 197–210.
- Gavião MB, Engelen L & Van Der Bilt A (2004) Chewing behavior and salivary secretion. Eur J Oral Sci 112: 19–24.
- Geetha C, Venkatesh SG, Dunn BH & Gorr SU (2003) Expression and anti-bacterial activity of human parotid secretory protein (PSP). Biochem Soc T 31: 815–818.
- Genuit T, Bochicchio G, Napolitano LM, McCarter RJ & Roghman MC (2001) Prophylactic chlorhexidine oral rinse decreases ventilator-associated pneumonia in surgical ICU patients. Surg Infect (Larchmt) 2: 5–18.
- Gilbert P, Das J & Foley I (1997) Biofilm susceptibility to antimicrobials. Adv Dent Res 11: 160–167.
- Gjermansen M, Ragas P, Sternberg C, Molin S & Tolker-Nielsen T (2005) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol 7: 894–906.
- Gleeson M, Hall ST, Mcdonald WA, Flanagan AJ & Clancy RL (1999) Salivary IgA subclasses and infection risk in elite swimmers. Immunol Cell Biol 77: 351–355.
- Gosney MA, Preston AJ, Corkhill J, Millns B & Martin MV (1999) Pseudomonas aeruginosa septicaemia from an oral source. Brit Dent J 187: 639–640.
- Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, Pot B, Hartung T, Hols P & Mercenier A (2005) Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. P Natl Acad Sci USA 102: 10321–10326.
- Guivante-Nabet C, Berenholc C & Berdal A (1999) Caries activity and associated risk factors in elderly hospitalised population – 15-months follow-up in French institutions. Gerodontology 16: 47–58.
- Handfield M, Baker HV & Lamont RJ (2008) Beyond good and evil in the oral cavity: insights into host–microbe relationships derived from transcriptional profiling of gingival cells. J Dent Res 87: 203–223.
- Haraszthy VI, Zambon JJ, Trevisan M, Zeid M & Genco RJ (2000) Identification of periodontal pathogens in atheromatous plaques. J Periodontol 71: 1554–1560.
- Hardy GG, Tudor SM & St Geme JW III (2003) The pathogenesis of disease due to nontypeable Haemophilus influenzae. Methods Mol Med 71: 1–28.
- Hase JC (1993) Influence of age and salivary secretion rate on oral sugar clearance. Swed Dent J Suppl 89: 1–65.
- Hasegawa Y, Mans JJ, Mao S, Lopez MC, Baker HV, Handfield M & Lamont RJ (2007) Gingival epithelial cell transcriptional responses to commensal and opportunistic oral microbial species. Infect Immun 75: 2540–2547.
- Haukioja A, Yli-Knuuttila H, Loimaranta V, Kari K, Ouwehand AC, Meurman JH & Tenovuo J (2006) Oral adhesion and survival of probiotic and other lactobacilli and bifidobacteria in vitro. Oral Microbiol Immun 21: 326–332.
- Heo SM, Haase EM, Lesse AJ, Gill SR & Scannapieco FA (2008) Genetic relationships between respiratory pathogens isolated from dental plaque and bronchoalveolar lavage fluid from patients in the intensive care unit undergoing mechanical ventilation. Clin Infect Dis 47: 1562–1570.
- Higuchi M, Yamamoto Y & Kamio Y (2000) Molecular biology of oxygen tolerance in lactic acid bacteria: functions of NADH oxidases and Dpr in oxidative stress. J Biosci Bioeng 90: 484–493.
- Hogan DA & Kolter R (2002) Pseudomonas–Candida interactions: an ecological role for virulence factors. Science 21: 2229–2232.
- Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG & Gordon JI (2001) Molecular analysis of commensal host–microbial relationships in the intestine. Science 291: 881–884.
- Horz HP, Meinelt A, Houben B & Conrads G (2007) Distribution and persistence of probiotic Streptococcus salivarius K12 in the human oral cavity as determined by real-time quantitative polymerase chain reaction. Oral Microbiol Immun 22: 126–130.
- Hunt SM, Werner EM, Huang B, Hamilton MA & Stewart PS (2004) Hypothesis for the role of nutrient starvation in biofilm detachment. Appl Environ Microb 70: 7418–7425.
- Ikebe K, Matsuda KI, Morii K, Hazeyama T, Kagawa R, Ogawa T & Nokubi T (2007) Relationship between bite force and salivary flow in older adults. Oral Surg Oral Med O 104: 510–515.
- Jack RW, Tagg JR & Ray B (1995) Bacteriocins of gram-positive bacteria. Microbiol Rev 59: 171–200.
- Janssens JP (2005) Pneumonia in the elderly (geriatric) population. Curr Opin Pulm Med 11: 226–230.
- Javier RM, Sibilia J, Lugger AS, Natarajan-Ame S, Kuntz JL & Jerbrecht R (2001) Fatal Aspergillus fumigatus myositis in an immunocompetent patient. Eur J Clin Microbiol 20: 810–813.
- Jenkinson HF (1994) Cell surface protein receptors in oral streptococci. FEMS Microbiol Lett 121: 133–140.
- Jenkinson HF & Lamont RJ (1997) Streptococcal adhesion and colonization. Crit Rev Oral Biol M 8: 175–200.
- Jia R, Guo JH, Fan MW, Bian Z, Chen Z, Peng B & Fan B (2004) Mucosal immunization against dental caries with plasmid DNA encoding pac gene of Streptococcus mutans in rats. Vaccine 22: 2511–2516.
- Kamaguchi A, Nakayama K, Ichiyama S, Nakamura R, Watanabe T, Ohta M, Baba H & Ohyama T (2003) Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms. Curr Microbiol 47: 485–491.
- Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AG, Pettersson S & Conway S (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5: 104–112.
- Kilian M & Schiott CR (1975) Haemophilii and related bacteria in the human oral cavity. Arch Oral Biol 20: 791–796.
- Kimizuka R, Kato T, Ishihara K & Okuda K (2003) Mixed infections with Porphyromonas gingivalis and Treponema denticola cause excessive inflammatory responses in a mouse pneumonia model compared with monoinfections. Microbes Infect 5: 1357–1362.
- Kinniment SL, Wimpenny JW, Adams D & Marsh PD (1996) The effect of chlorhexidine on defined, mixed culture oral biofilms grown in a novel model system. J Appl Bacteriol 81: 120–125.
- Kiyak HA, Grayston MN & Crinean CL (1993) Oral health problems and needs of nursing home residents. Community Dent Oral 21: 49–52.
- Klausen M, Gjermansen M, Kreft JU & Tolker-Nielsen T (2006) Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol Lett 261: 1–11.
- Klentrou P, Cieslak T, MacNeil M, Vintinner A & Plyley M (2002) Effect of moderate exercise on salivary immunoglobulin A and infection risk in humans. Eur J Appl Physiol 87: 153–158.
- Koeman M, Van Der Ven AJ, Hak E et al. (2006) Oral decontamination with chlorhexidine reduces the incidence of ventilator-associated pneumonia. Am J Resp Crit Care 173: 1348–1355. Comment in: ACP J Club145: 68, 2006. Am J Resp Crit Care173: 1297–1298, 2006. Am J Resp Crit Care175: 418, 2007. Evid Based Nurs10: 19, 2007.
- Kolenbrander PE (2000) Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol 54: 413–437.
- Kolenbrander PE, Andersen RN & Moore LV (1990) Intrageneric coaggregation among strains of human oral bacteria: potential role in primary colonization of the tooth surface. Appl Environ Microb 56: 3890–3894.
- Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS & Palmer RJ Jr (2002) Communication among oral bacteria. Microbiol Mol Biol R 66: 486–505.
- Komiyama K & Gibbons RJ (1984) Interbacterial adherence between Actinomyces viscosus and strains of Streptococcus pyogenes, Streptococcus agalactiae, and Pseudomonas aeruginosa. Infect Immun 44: 86–90.
- Komiyama K, Tynan JJ, Habbick BF, Duncan DE & Liepert DJ (1985) Pseudomonas aeruginosa in the oral cavity and sputum of patients with cystic fibrosis. Oral Surg Oral Med O 59: 590–594.
- Komiyama K, Habbick BF & Gibbons RJ (1987) Interbacterial adhesion between Pseudomonas aeruginosa and indigenous oral bacteria isolated from patients with cystic fibrosis. Can J Microbiol 33: 27–32.
- Kosono S, Haga K, Tomizawa R, Kajiyama Y, Hatano K, Takeda S, Wakai Y, Hino M & Kudo T (2005) Characterization of a multigene-encoded sodium/hydrogen antiporter (sha) from Pseudomonas aeruginosa: its involvement in pathogenesis. J Bacteriol 187: 542–548.
- Krisanaprakornkit S, Kimball JR & Dale BA (2002) Regulation of human beta-defensin-2 in gingival epithelial cells: the involvement of mitogen-activated protein kinase pathways, but not the NF-kappaB transcription factor family. J Immunol 168: 316–324.
- Kumar A, Wu H, Collier-Hyams LS, Hansen JM, Li T, Yamoah K, Pan ZQ, Jones DP & Neish AS (2007) Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. EMBO J 26: 4457–4466.
- Lamm ME, Nedrud JG, Kaetzel CS & Mazanec MB (1995) IgA and mucosal defense. APMIS 103: 241–246.
-
Lamont RJ,
Hersey SG &
Rosan B (1992) Characterization of the adherence of Porphyromonasgingivalis to oral streptococci.
Oral Microbiol Immun
7: 193–197.
10.1111/j.1399-302X.1992.tb00024.x Google Scholar
- Lawrence HP (2002) Salivary markers of systemic disease: noninvasive diagnosis of disease and monitoring of general health. J Can Dent Assoc 68: 170–174.
- Lawrence HP, Fillery E, Matear DW, Paterson L, Hawkins RJ & Locker D (2001) The association between salivary sIgA, nutritional status, and functional dependence in the elderly. J Dent Res 80: 43 (AADR abstracts).
- Lee D, Howlett J, Pratten J, Mordan N, McDonald A, Wilson M & Ready D (2009) Susceptibility of MRSA biofilms to denture-cleansing agents. FEMS Microbiol Lett 291: 241–246.
- Lerrer B, Lesman-Movshovich E & Gilboa-Garber N (2005) Comparison of the antimicrobial adhesion potential of human body fluid glycoconjugates using fucose-binding lectin (PA-IIL) of Pseudomonas aeruginosa and Ulex europaeus lectin (UEA-I). Curr Microbiol 51: 202–206.
- Lesourd B (2004) Nutrition: a major factor influencing immunity in the elderly. J Nutr Health Aging 8: 28–37.
- Limeback H (1998) Implications of oral infections on systemic diseases in the institutionalized elderly with a special focus on pneumonia. Ann Periodontol 3: 262–275.
- Lindermann RA, Newman MG, Kaufman AK & Le TV (1985) Oral colonization and susceptibility testing of Pseudomonas aeruginosa oral isolates from cystic fibrosis patients. J Dent Res 64: 54–57.
- Liong MT (2008) Safety of probiotics: translocation and infection. Nutr Rev 66: 192–202.
- Lund B, Edlund C, Rynnel-Dagöö B, Lundgren Y, Sterner J & Nord CE (2001) Ecological effects on the oro- and nasopharyngeal microflora in children after treatment of acute otitis media with cefuroxime axetil or amoxycillin-clavulanate as suspensions. Clin Microbiol Infec 7: 230–237.
- MacEntee MI (2006) Missing links in oral health care for frail elderly people. J Can Dent Assoc 72: 421–425.
- MacFarlane TW (1984) The oral ecology of patients with severe Sjögren's syndrome. Microbios 41: 99–106.
- Marcotte H & Lavoie MC (1998) Oral microbial ecology and the role of salivary immunoglobulin A. Microbiol Mol Biol R 62: 71–109.
- Marik PE & Kaplan D (2003) Aspiration pneumonia and dysphagia in the elderly. Chest 124: 328–336.
- Marsh PD (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149: 279–294.
- Marsh PD (2004) Dental plaque as a microbial biofilm. Caries Res 38: 204–211.
- Marsh PD (2005) Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol 32 (suppl 6): 7–15.
- Marsh PD (2009) Dental plaque as a biofilm: the significance of pH in health and caries. Compend Contin Educ Dent 30: 76–78, 80, 83–87; quiz 88, 90.
- Marsh PD & Percival RS (2006) The oral microflora – friend or foe? Can we decide? Int Dent J 56 (suppl 1): 233–239.
- Matsumoto T, Ishikawa H, Tateda K, Yaeshima T, Ishibashi N & Yamaguchi K (2008) Oral administration of Bifidobacterium longum prevents gut-derived Pseudomonas aeruginosa sepsis in mice. J Appl Microbiol 104: 672–680.
- Mazmanian SK, Round JL & Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453: 620–625.
- McNabb PC & Tomasi TB (1981) Host defense mechanisms at mucosal surfaces. Annu Rev Microbiol 35: 477–496.
- Mojon P (2002) Oral health and respiratory infection. J Can Dent Assoc 68: 340–345.
- Mojon P & MacEntee MI (1994) Estimates of time and propensity for dental treatment among institutionalised elders. Gerodontology 11: 99–107.
- Nederfors T, Isaksson R, Mörnstad H & Dahlöf C (1997) Prevalence of perceived symptoms of dry mouth in an adult Swedish population – relation to age, sex and pharmacotherapy. Community Dent Oral 25: 211–216.
- Neish AS, Gewirtz AT, Zeng H, Young AN, Hobert ME, Karmali V, Rao AS & Madara JL (2000) Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 289: 1560–1563.
- Nord CE & Heimdahl A (1986) Impact of orally administered antimicrobial agents on human oropharyngeal and colonic microflora. J Antimicrob Chemoth 18 (suppl C): 159–164.
- Nord CE, Heimdahl A, Lundberg C & Marklund G (1987) Impact of cefaclor on the normal human oropharyngeal and intestinal microflora. Scand J Infect Dis 19: 681–685.
- Nord CE, Sillerström E & Wahlund E (2006) Effect of tigecycline on normal oropharyngeal and intestinal microflora. Antimicrob Agents Ch 50: 3375–3380.
- Nguyen PT, Abranches J, Phan TN & Marquis RE (2002) Repressed respiration of oral streptococci grown in biofilms. Curr Microbiol 44: 262–266.
- O'Hara AM, O'Regan P, Fanning A, O'Mahony C, Macsharry J, Lyons A, Bienenstock J, O'Mahony L & Shanahan F (2006) Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118: 202–215.
- Okuda K, Kimizuka R, Abe S, Kato T & Ishihara K (2005) Involvement of periodontopathic anaerobes in aspiration pneumonia. J Periodontol 76 (suppl): 2154–2160.
- Otto M (2008) Staphylococcal biofilms. Curr Top Microbiol 322: 207–228.
- Packer S, Woodley N, Wilson M & Mullany P (1999) Prevalence and persistence of amoxycillin-resistant bacteria in the dental plaques of adults. Microbios 100: 135–144.
- Pan Y, Teng D, Burke AC, Haase EM & Scannapieco FA (2009) Oral bacteria modulate invasion and induction of apoptosis in HEp-2 cells by Pseudomonas aeruginosa. Microb Pathogenesis 46: 73–79.
- Parsek MR & Tolker-Nielsen T (2008) Pattern formation in Pseudomonas aeruginosa biofilms. Curr Opin Microbiol 11: 560–566.
- Paul M, Soares-Weiser K & Leibovici L (2003) Beta lactam monotherapy versus beta lactam-aminoglycoside combination therapy for fever with neutropenia: systematic review and meta-analysis. BMJ 326: 1111.
- Pedersen BK & Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 80: 1055–1081.
- Piper C, Draper LA, Cotter PD, Ross RP & Hill C (2009) A comparison of the activities of lacticin 3147 and nisin against drug-resistant Staphylococcusaureus and Enterococcus species. J Antimicrob Chemother 64: 546–551.
- Prakobphol A, Murray PA & Fisher SJ (1987) Bacterial adherence on replicas of sodium dodecyl sulfate-polyacrylamide gels. Anal Biochem 164: 5–11.
- Pratten J & Wilson M (1999) Antimicrobial susceptibility and composition of microcosm dental plaques supplemented with sucrose. Antimicrob Agents Ch 43: 1595–1599.
- Preston AJ, Kearns A, Barber MW & Gosney MA (2006) The knowledge of healthcare professionals regarding elderly persons' oral care. Brit Dent J 201: 293–295.
- Pugin J, Auckenthaler R, Lew DP & Suter PM (1991) Oropharyngeal decontamination decreases incidence of ventilator-associated pneumonia. A randomized, placebo-controlled, double-blind clinical trial. JAMA 265: 2704–2710.
- Quirynen M, Teughels W & Van Steenberghe D (2003) Microbial shifts after subgingival debridement and formation of bacterial resistance when combined with local or systemic antimicrobials. Oral Dis 9 (suppl 1): 30–37.
- Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S & Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229–241.
- Rautava S & Walker WA (2007) Commensal bacteria and epithelial cross talk in the developing intestine. Curr Gastoenterol Rep 9: 385–392.
- Ready D, Bedi R, Spratt DA, Mullany P & Wilson M (2003) Prevalence, proportions, and identities of antibiotic-resistant bacteria in the oral microflora of healthy children. Microb Drug Resist 9: 362–372.
- Reed R, Broder HL, Jenkins G, Spivack E & Janal MN (2006) Oral health promotion among older persons and their care providers in a nursing home facility. Gerodontology 23: 73–78.
- Rosan B & Lamont RJ (2000) Dental plaque formation. Microbes Infect 2: 1599–1607.
- Rosenthal S & Tager IB (1975) Prevalence of gram-negative rods in the normal pharyngeal flora. Ann Intern Med 83: 355–357.
- Ruhl S, Sandberg AL & Cisar JO (2004) Salivary receptors for the proline-rich protein-binding and lectin-like adhesins of oral actinomyces and streptococci. J Dent Res 83: 505–510.
- Russell SL, Boylan RJ, Kaslick RS, Scannapieco FA & Katz RV (1999) Respiratory pathogen colonization of the dental plaque of institutionalized elders. Spec Care Dentist 19: 128–134.
- Sakamoto Y, Ueki S, Kasai T, Takato J, Shimanuki H, Honda H, Ito T & Haga H (2009) Effect of exercise, aging and functional capacity on acute secretory immunoglobulin A response in elderly people over 75 years of age. Geriatr Gerontol Int 9: 81–88.
- Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG & Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186: 7312–7326.
- Sbordone L & Bortolaia C (2003) Oral microbial biofilms and plaque-related diseases: microbial communities and their role in the shift from oral health to disease. Clin Oral Invest 7: 181–188.
- Scannapieco FA (1999) Role of oral bacteria in respiratory infection. J Periodontol 70: 793–802.
- Scannapieco FA & Mylotte JM (1996) Relationships between periodontal disease and bacterial pneumonia. J Periodontol 67 (suppl): 1114–1122.
- Scannapieco FA, Stewart EM & Mylotte JM (1992) Colonization of dental plaque by respiratory pathogens in medical intensive care patients. Crit Care Med 20: 740–745.
- Scannapieco FA, Papandonatos GD & Dunford RG (1998) Associations between oral conditions and respiratory disease in a national sample survey population. Ann Periodontol 3: 251–256.
- Scannapieco FA, Bush RB & Paju S (2003) Associations between periodontal disease and risk for nosocomial bacterial pneumonia and chronic obstructive pulmonary disease. A systematic review. Ann Periodontol 8: 54–69.
- Schenkels LC, Ligtenberg AJ, Veerman EC & Van Nieuw Amerongen A (1993) Interaction of the salivary glycoprotein EP-GP with the bacterium Streptococcus salivarius HB. J Dent Res 72: 1559–1565.
- Schenkels LC, Veerman EC & Nieuw Amerongen AV (1995) Biochemical composition of human saliva in relation to other mucosal fluids. Crit Rev Oral Biol M 6: 161–175.
- Schleheck D, Barraud N, Klebensberger J, Webb JS, McDougald D, Rice SA & Kjelleberg S (2009) Pseudomonas aeruginosa PAO1 preferentially grows as aggregates in liquid batch cultures and disperses upon starvation. PLoS ONE 4: e5513.
- Schreiner A (1983) Anaerobic pulmonary infections. Scand J Gastroentero 85 (suppl): 55–59.
- Senpuku H, Sogame A, Inoshita E, Tsuha Y, Miyazaki H & Hanada N (2003) Systemic disease in association with microbial species in oral biofilm from elderly requiring care. Gerontology 49: 301–309.
- Shimizu K, Kimura F, Akimoto T, Akama T, Kuno S & Kono I (2007a) Effect of free-living daily physical activity on salivary secretory IgA in elderly. Med Sci Sport Exer 39: 593–598.
- Shimizu K, Kimura F, Akimoto T, Akama T, Otsuki T, Nishijima T, Kuno S & Kono I (2007b) Effects of exercise, age and gender on salivary secretory immunoglobulin A in elderly individuals. Exerc Immunol Rev 13: 55–66.
- Shirtliff ME, Peters BM & Jabra-Rizk MA (2009) Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett 299: 1–8.
- Siqueira JF Jr, Rôças IN, Oliveira JC & Santos KR (2001) Detection of putative oral pathogens in acute periradicular abscesses by 16S rDNA-directed polymerase chain reaction. J Endodont 27: 164–167.
- Slack E, Hapfelmeier S, Stecher B et al. (2009) Innate and adaptive immunity cooperate flexibly to maintain host–microbiota mutualism. Science 325: 617–620.
- Smith DJ & Mattos-Graner RO (2008) Secretory immunity following mutans streptococcal infection or immunization. Curr Top Microbiol 319: 131–156.
- Socransky SS, Smith C & Haffajee AD (2002) Subgingival microbial profiles in refractory periodontal disease. J Clin Periodontol 29: 260–268.
- Sreebny LM & Schwartz SS (1997) A reference guide to drugs and dry mouth – 2nd edition. Gerodontology 14: 33–47.
- Stark CA, Adamsson I, Edlund C, Sjösted S, Seensalu R, Wikström B & Nord CE (1996) Effects of omeprazole and amoxycillin on the human oral and gastrointestinal microflora in patients with Helicobacter pylori infection. J Antimicrob Chemoth 38: 927–939.
- Stewart PS & Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358: 135–138.
- Stjernquist-Desatnik A, Samuelsson P & Walder M (1993) Penetration of penicillin V to tonsillar surface fluid in healthy individuals and in patients with acute tonsillitis. J Laryngol Otol 107: 309–312.
- Swartz TH, Ito M, Ohira T, Natsui S, Hicks DB & Krulwich TA (2007) Catalytic properties of Staphylococcus aureus and Bacillus members of the secondary cation/proton antiporter-3 (Mrp) family are revealed by an optimized assay in an Escherichia coli host. J Bacteriol 189: 3081–3090.
- Sweeney MP, Williams C, Kennedy C, Macpherson LM, Turner S & Bagg J (2007) Oral health care and status of elderly care home residents in Glasgow. Community Dent Hlth 24: 37–42.
- Tada A, Hanada N & Tanzawa H (2002a) The relation between tube feeding and Pseudomonas aeruginosa detection in the oral cavity. J Gerontol A-Biol 57: M71–M72.
- Tada A, Watanabe T, Yokoe H, Hanada N & Tanzawa H (2002b) Oral bacteria influenced by the functional status of the elderly people and the type and quality of facilities for the bed-ridden. J Appl Microbiol 93: 487–491.
- Tada A, Shiiba M, Yokoe H, Hanada N & Tanzawa H (2004) Relationship between oral motor dysfunction and oral bacteria in bedridden elderly. Oral Surg Oral Med O 98: 184–188.
- Tada A, Senpuku H, Motozawa Y, Yoshihara A, Hanada N & Tanzawa H (2006) Association between commensal bacteria and opportunistic pathogens in the dental plaque of elderly individuals. Clin Microbiol Infec 12: 776–781.
- Tawara Y, Honma K & Naito Y (1996) Methicillin-resistant Staphylococcus aureus and Candida albicans on denture surfaces. Bull Tokyo Dent Coll 37: 119–128.
- Terpenning MS, Taylor GW, Lopatin DE, Kerr CK, Dominguez BL & Loesche WJ (2001) Aspiration pneumonia: dental and oral risk factors in an older veteran population. J Am Geriatr Soc 49: 557–563.
- Tien MT, Girardin SE, Regnault B, Le Bourhis L, Dillies MA, Coppee JY, Bourdet-Sicard R, Sansonetti PJ & Pedron T (2006) Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 176: 1228–1237.
- Tong H, Zhu B, Chen W, Qi F, Shi W & Dong X (2006) Establishing a genetic system for ecological studies of Streptococcus oligofermentans. FEMS Microbiol Lett 264: 213–219.
- Traub WH & Spohr M (1983) Hydrogen peroxide-mediated antagonism against Serratia marcescens by Streptococcus mitis. Zentralbl Bakteriol Mikrobiol Hyg [A] 254: 326–332.
- Tsuji M, Suzuki K, Kinoshita K & Fagarasan S (2008) Dynamic interactions between bacteria and immune cells leading to intestinal IgA synthesis. Semin Immunol 20: 59–66.
- Turner MD & Ship JA (2007) Dry mouth and its effects on the oral health of elderly people. J Am Dent Assoc 138 (suppl): 15S–20S.
- Uehara Y, Kikuchi K, Nakamura T, Nakama H, Agematsu K, Kawakami Y, Maruchi N & Totsuka K (2001a) Inhibition of methicillin-resistant Staphylococcus aureus colonization of oral cavities in newborns by viridans group streptococci. Clin Infect Dis 32: 1399–1407.
- Uehara Y, Kikuchi K, Nakamura T, Nakama H, Agematsu K, Kawakami Y, Maruchi N & Totsuka K (2001b) H2O2 produced by viridans group streptococci may contribute to inhibition of methicillin-resistant Staphylococcus aureus colonization of oral cavities in newborns. Clin Infect Dis 32: 1408–1413.
- Uehara Y, Agematsu K, Kikuchi K et al. (2006) Secretory IgA, salivary peroxidase, and catalase-mediated microbicidal activity during hydrogen peroxidase catabolism in viridans streptococci: pathogen coaggregation. J Infect Dis 194: 98–107.
- Vasen W & Fiorentino R (2003) Antibiotics effects on intestinal flora: its modifications with the antibiotics used in the clinical practice of gastroenterology. Acta Gastroen Latam 33: 37–41.
- Vergona KD (2005) A self-reported survey of Alzheimer's centers in Southwestern Pennsylvania. Spec Care Dentist 25: 164–170.
- Wårdh I, Hallberg LR, Berggren U, Andersson L & Sörensen S (2003) Oral health education for nursing personnel; experiences among specially trained oral care aides: one-year follow-up interviews with oral care aides at a nursing facility. Scand J Caring Sci 17: 250–256.
- Watanabe S & Dawes C (1988) A comparison of the effects of tasting and chewing foods on the flow rate and composition. Arch Oral Biol 33: 761–764.
- Weng M & Walker WA (2006) Bacterial colonization, probiotics, and clinical disease. J Pediatr 149: S107–S114.
- Whittaker CJ, Klier CM & Kolenbrander PE (1996) Mechanisms of adhesion by oral bacteria. Annu Rev Microbiol 50: 513–552.
- Wikner S & Soder PO (1994) Factors associated with salivary buffering capacity in young adults in Stockholm, Sweden. Scand J Dent Res 102: 50–53.
- Wilson M (1996) Susceptibility of oral bacterial biofilms to antimicrobial agents. J Med Microbiol 44: 79–87.
- Wüst J & Hardegger U (1993) Penetration of clarithromycin into human saliva. Chemotherapy 39: 293–296.
- Yao ES, Lamont RJ, Leu SP & Weingerg A (1996) Interbacterial binding among strains of pathogenic and commensal oral bacterial species. Oral Microbiol Immun 11: 35–41.
- Yoneyama T, Yoshida M, Matsui T & Sasaki H (1999) Oral care and pneumonia. Lancet 354: 515.
- Zhou HH, Chan YP, Arnold K & Sun M (1985) Single-dose pharmacokinetics of ceftriaxone in healthy Chinese adults. Antimicrob Agents Ch 27: 192–196.