Open Access

Tobacco use increases susceptibility to bacterial infection

Tobacco Induced Diseases20084:12

https://doi.org/10.1186/1617-9625-4-12

Received: 03 July 2008

Accepted: 18 December 2008

Published: 18 December 2008

Abstract

Active smokers and those exposed to secondhand smoke are at increased risk of bacterial infection. Tobacco smoke exposure increases susceptibility to respiratory tract infections, including tuberculosis, pneumonia and Legionnaires disease; bacterial vaginosis and sexually transmitted diseases, such as chlamydia and gonorrhoea; Helicobacter pylori infection; periodontitis; meningitis; otitis media; and post-surgical and nosocomial infections. Tobacco smoke compromises the anti-bacterial function of leukocytes, including neutrophils, monocytes, T cells and B cells, providing a mechanistic explanation for increased infection risk. Further epidemiological, clinical and mechanistic research into this important area is warranted.

Review

It is well established that smokers are more susceptible than non-smokers to a plethora of chronic diseases and conditions that include stroke, vascular diseases, chronic obstructive pulmonary disease, multiple cancers, periodontal diseases, hypertension, impotence and osteoporosis. However, smokers are also significantly more susceptible to multiple bacterial infections than are non-smokers. Such infections can be life-threatening and both active smokers as well as those exposed to secondhand smoke toxins are at increased risk. This important relationship between smoking and ill-health may not be universally appreciated. Therefore, we set out to review and summarize the evidence associating tobacco smoke exposure with bacterial infections and to introduce interactions between tobacco smoke, bacteria, and the immune system that may help explain the increased susceptibility to infectious disease in smokers.

Bacterial infections associated with tobacco smoking

Nasopharyngeal and respiratory tract infections

Adult smokers are at increased risk of respiratory infection by several bacterial pathogens, including Streptococcus pneumonia, Neisseria meningitidis, Haemophilus influenzae and Legionella pneumophila [15]. Brook and Gober reported that the nasopharyngeal microflora of smokers contains fewer normal bacteria (such as α-hemolytic and nonhemolytic streptococci, and Prevotella and Peptostreptococcus species) that can interfere with colonization by selected pathogens (S. pneumoniae, H. influenzae (non-type b), Moraxella catarrhalis, and Streptococcus pyogenes) and that the nasopharyngeal microflora also contains more potential pathogens compared with those of nonsmokers[6]. Such increased carriage of potentially pathogenic species of bacteria in both adults and children was hypothesized [6] to possibly be due to enhanced bacterial binding to the epithelial cells of smokers [7] and the low number of α-hemolytic streptococci with inhibitory activity against S. pyogenes in the oral cavities of smokers [6, 8]. More recently, the same group followed a small number of quitters (n = 20) for a period of up to 15 months post-tobacco cessation, and concluded that the high number of pathogens (S. pneumoniae, H. influenzae, M. catarrhalis, and S. pyogenes) and low number of interfering organisms found in the nasopharynx of smokers reverted to normal levels after stopping smoking [9].

When comparing patients with stable chronic obstructive pulmonary disease (COPD) with healthy controls (normal spirometry and chest radiography) Zalacain et al found current smoking to be associated (OR 3.17, 95% CI 2.50–8.00) with pulmonary infection with pathogenic bacteria – H. influenzae, Streptococcus viridans, S. pneumoniae and M. catarrhalis being the most frequently cultured species [10]. In patients with chronic obstructive pulmonary disease (COPD), bacterial exacerbations are also more prevalent among current smokers (OR 3.77, 95% CI 1.17–12.12) [11, 12].

Several studies indicate that exposure to passive smoking also increases the incidence of sneezing, sore throat, cough, and frequent cough [13, 14]. The incidence of group A streptococcus sore throat has been reported to be higher among children living in homes that include a tobacco smoker [15]. Thus, there is a consistent body of literature showing a significant association between tobacco smoke exposure and respiratory tract infections. More specific pulmonary diseases are now considered.

Cystic Fibrosis

Cystic fibrosis is a life-shortening autosomal recessive disease affecting the pulmonary, gastrointestinal and genitourinary systems. Lung colonization with a succession of pathogens, such as Staphylococcus aureus and H. influenzae is likely to occur in affected individuals. Ultimately, persistent colonization by the opportunistic pathogen Pseudomonas aeruginosa contributes to significant morbidity and mortality in cystic fibrosis [16]. Epidemiological studies have shown that secondhand smoke exposure is associated with poor prognosis in cystic fibrosis patients [17] and that a dose-dependent relationship exists between number of cigarettes smoked and severity of disease amongst young patients [18]. In keeping with these data, mice infected with P. aeruginosa and exposed to tobacco smoke exhibit delayed clearance of infection and increased morbidity compared to control mice which were infected but not exposed to smoke [19].

Pneumonia, Legionnaires' disease and bronchitis

Several studies have shown smoking to be significantly associated with the development of bronchitis and bacterial pneumonia [20]. There are dose-response relations between the current number of cigarettes smoked per day; pack-years of smoking; and time since quitting and invasive pneumococcal disease, with approximately 50% of those with invasive pneumococcal disease being cigarette smokers [2]. Recently, several authors have discussed the possibility of recommending the routine extension of pneumococcal vaccine coverage to current smokers [21, 22]. There is also strong evidence that smoking is an independent risk factor for Legionnaires disease, an atypical pneumonia that usually develops 2 to 14 days after exposure to Legionella pneumophila [5, 23]. Complications of Legionnaires' disease can be severe and include respiratory failure, septic shock, and acute kidney failure. Indeed, mortality rates as high as 8.2–13.5% have been reported in infected individuals among the general populations of several European countries [24, 25]. Studies indicate a dose dependent relationship between frequency of Legionnaires disease and passive smoking in children [26] as well as in adult smokers [27].

Tuberculosis

More than 30% of world's population may be infected with the bacterial agent of tuberculosis, Mycobacterium tuberculosis. Tuberculosis represents the leading cause of death from infectious disease worldwide and the leading cause of death among HIV-positive individuals [28]. Smoking increases susceptibility to bacillary tuberculosis in a dose-dependent manner [29, 30], adversely affects clinical manifestations [31], and accounts for 12% of all tuberculosis deaths [28]. The disease progresses more rapidly in smokers than in non-smokers, while smoking is also associated with increased relapse and mortality [32]. Quitting smoking and prevention of exposure to secondhand smoke are both important measures in the control of tuberculosis [33]. Indeed, the W.H.O. has estimated that, in China, heavy smoking (> 20 cigarettes per day) leads to a doubling of the death rate from tuberculosis [28].

Bacterial meningitis

Carriage of H. influenzae, pneumococcus, and meningococcus has been shown to be more common in both active and second-hand smokers than in nonsmokers [3438]. Indeed, the relationship may be dose-dependent and, in a study of military recruits, smoke exposure gave an attributable risk for meningococcal carriage of 33% [38]. In addition to increased carriage, meningitis cases have a two-to fourfold higher risk of exposure to cigarette smoke than controls [34]. Furthermore, second-hand smoke exposure predisposes to nasopharyngeal colonization with specific Staphylococcus aureus variants that may have altered capacity to compete with pneumococci subtypes [39]. Passive exposure to tobacco smoke has also been associated with Hemophilus influenzae and pneumococcus meningitis in Australian children [4].

Vaginosis and sexually transmitted infections

Bacterial vaginosis, although often asymptomatic, can cause considerable discomfort and is associated with the development of more serious infections, such as septicemia and increased risk of poor pregnancy outcome [4042]. Tobacco smoking has been significantly correlated with bacterial vaginosis, typically being in the region of twice as common in smokers as non-smokers, with a greater prevalence noted in young women [4345]. Tobacco use has also been independently associated with a higher prevalence of specific sexually-transmitted bacterial infections – chlamydia and gonorrhoea [46].

Helicobacter pylori infection

There are several factors that may contribute to an increased susceptibility to gastric and duodenal ulcers in smokers compared to non-smokers. Smoking decreases antacid (bicarbonate) secretion from the pancreas, while stimulating gastric acid secretion [47, 48]. Furthermore, the great majority of gastric and duodenal ulcers are associated with H. pylori infection and smokers are more susceptible than non-smokers to gastrointestinal infection with this bacterial species [4951]. Additionally, smoking has been significantly associated with the failure of anti-H. pylori therapy [52, 53].

Periodontitis

Patients who smoke exhibit not only increased susceptibility to periodontitis but are also more likely than non-smokers to display severe disease and to be refractory to treatment [54]. Despite some conflicting data that smoking may not influence the sub-gingival micoflora [5558], the balance of recent data strongly suggests that tobacco-induced susceptibility to periodontitis is associated with shifts in the microbial composition of complex periodontal plaque communities smokers [51, 5966], as we have recently reviewed [54]. For example, Zambon et al showed a higher prevalence of Aggregatibacter actinomycetemcomitans, Tannerella forsythia and Porphyromonas gingivalis in smokers [59]. Umeda et al [63] reported an increased risk for harbouring Treponema denticola in smokers. Haffajee and Socransky [67] showed an increased prevalence of eight species, including P. gingivalis, in current smokers, while Eggert et al [62] have shown a higher prevalence and proportion of T. forsythia, Campylobacter rectus, P. gingivalis and Peptostreptococcus micros in plaque samples from smokers.

Inflammatory bowel diseases

Of all the factors associated with inflammatory bowel diseases, the most solid evidence is for smoking and enteric bacterial flora – and these two risk factors may well be related [68]. Smoking increases the risk of Crohn's disease and worsens its clinical course, but has a protective effect in ulcerative colitis [68], as we and others have recently reviewed [6971]. Furthermore, in ulcerative colitis patients, ex-smokers are more likely than current smokers to exhibit increased disease progression, more frequent hospitalization, and are twice as likely as current smokers to require colectomy [72]. However, in Crohn's disease patients, smokers exhibit higher disease recurrence rates, require more frequent surgical interventions, and have a greater need for immunosuppressive agents compared to non-smokers [72].

Otitis media

Otitis media is an infection of the middle ear, commonly caused by Moraxella catarrhalis, S. pneumoniae and H. influenzae, that is rarely associated with severe complications, such as hearing loss and meningitis. The posterior nasopharynx flora of parents who smoke, compared to the flora of non-smoking parents, contains more potential pathogens similar to those recovered from otitis media-prone children [73]. Additionally, children exposed to secondhand smoke are more susceptible to otitis media [1]. Indeed, secondhand smoke has been estimated to be responsible for 0.7 to 1.6 million physician visits for middle ear infections annually in the USA alone [74].

Post-Surgical and nosocomial infections

As many as 5% of patients undergoing surgery develop surgical site infections, which leads to significant morbidity and may sometimes be fatal [75]. Smoking is known to be an important patient-related risk factor for surgical site infections [75, 76]. Smoking also increases the risk of nosocomial non-wound infections, bacteremia and urinary tract infections with multiple bacterial species and worsens bacteremic prognosis [7780].

In utero and neonatal second-hand smoke exposure, neonatal infection and sudden infant death syndrome (SIDS)

12% of US women smoke during pregnancy [81] and, conservatively, 50% of US children are exposed to secondhand smoke [82, 83]. Maternal smoking has been associated with significantly higher rates of neonatal infection than found in the children of non-smoking mothers [82, 84, 85]. Furthermore, the odds ratios for SIDS in secondhand smoke-exposed neonates have risen considerably since the broad acceptance of "back-to-sleep" positioning [82]. It has recently been postulated that these two facts may be related and that SIDS could be caused by the interactions between components of cigarette smoke and infectious bacterial loads that would normally be sub-lethal in neonates that have not been exposed to tobacco smoke [82, 8688].

Mechanisms of increased susceptibility to bacterial infections in smokers

There is a large and productive tobacco research literature that focuses on epidemiology, behavior, addiction and quitting. However, despite the wealth of epidemiological evidence of the profound ill-effects of smoking on human health, studies that set out to understand the mechanisms of how cigarette smoke induces disease are limited, as we have recently commented [89]. It is not the intent of this review to provide comprehensive data on why tobacco use leads to increased rates of infectious disease in smokers. Rather, we will introduce some of the key potential mechanisms underlying this increased susceptibility and provide the reader with links to more exhaustive literature reviews.

Cigarette smoking can, theoretically, increase the risk of infection by pathogenic or opportunistic bacteria by three general mechanisms:

  • Tobacco-induced physiological and structural changes in humans.

  • Tobacco-induced increase in bacterial virulence.

  • Tobacco-induced dysregulation of immune function.

Such mechanisms are not mutually exclusive and all three may occur simultaneously. For example, tobacco smoke exposure may play a direct role in bacterial colonization of the respiratory tract by hindering mucociliary clearance of bacteria [19, 90]; while inducing bacterial components that aid in the binding of microbes to respiratory epithelial cells ([7] and our own, unpublished data); and concurrently decreasing the ability of respiratory phagocytic cells to detect and destroy pathogenic microbes [91]. Tobacco-induced physiological and structural changes in humans have focused primarily on the vasculature and respiratory tract. The vasoactive effects of cigarette smoke and nicotine appear to vary in different vascular beds. For example, smoking induces vasoconstriction in peripheral arteries [92] but vasodilation in cerebral blood vessels [93]. In periodontal tissues smoking does not seem to exert an acute vasoactive (constriction or dilation) influence on the microvasculature [94]. Rather, smoking results in a suppression of periodontal angiogenesis [95] in a manner that is rapidly reversible on smoking cessation [96]. Thus, the negative influence of smoking on mucociliary function most likely contributes to increased risk of bacterial infection by reducing the ability of the respiratory tract to clear pathogens, while the vasoconstrictive or anti-angiogenic influence of tobacco may contribute to increased susceptibility to bacterial infection by decreasing the effectiveness of inflammatory responses to pathogenic bacteria.

Several research groups have examined the interactions between infectious agents and cigarette smoke components. For example, Sayers et al. have demonstrated the potentiating influence of low levels of nicotine on staphylococcal and enterobacter toxins in studies addressing why passive exposure to cigarette smoke is a risk factor in sudden infant death syndrome [86, 87]. The same group has also shown that both nicotine and cotinine exhibit lethal synergy with toxins produced by several periodontal pathogens (Prevotella, Porphyromonas and Fusobacterium species) in the chick embryo toxicity model. Wiedeman et al. have suggested that tobacco smoke exposure may represent a risk for establishment of a chronic reservoir of C. pneumoniae infection within respiratory epithelium [97, 98]. Other groups have shown that exposure to cigarette smoke affects the growth of bacteria which may facilitate populational shifts in the microbial communities that colonize some human tissues. Zonuz et al reported that the growth of Streptococcus mutans and S. sanguis, two common oral bacteria, was stimulated by cigarette smoke [99]. In contrast, Ertel et al. showed that cigarette smoke inhibited the growth of Gram positive organisms, e.g., S. pneumoniae and S. aureus, but had little effect on Gram negative enteric bacteria such as Klebsiella, Enterobacter and Pseudomonas [100]. Consistent with this observation, they report that smokers have a propensity to develop heavy Gram negative colonization of the oral cavity relative to non-smokers. Interestingly, women who smoke are at higher risk of contracting bacterial vaginosis, as discussed above. Pavlova and Tao showed that the trace amounts of benzo [a]pyrene diol epoxide that are present in the vaginal secretions of women who smoke promotes the induction of bacteriophages in resident lactobacilli [101]. This may lead to a reduction in lactobacilli populations and facilitate overgrowth of anaerobes that are associated with vaginosis. In general, however, mechanistic studies to examine the direct influence of tobacco smoke on bacterial physiology and their pathogenic potential are lacking in the literature.

Dysregulation of innate immune function

Several innate cell receptor-tobacco agonist couples have been identified, suggesting that tobacco smoke is capable of effecting neutrophil and monocyte function both directly and indirectly [54, 102]. Indeed, multiple effector functions of professional phagocytic and antigen presenting innate cells (neutrophils, monocytes, macrophages and dendritic cells) are compromised by tobacco smoke. For example, in neutrophils, tobacco smoke and/or nicotine have been shown to reduce key anti-microbial activities including phagocytosis (the engulfment and uptake of bacteria) [54, 103, 104]; the generation of a respiratory burst (the combined oxygen-dependent processes by which neutrophils kill phagocytosed bacterial cells) [102, 105107]; and, ultimately, the ability to kill specific bacterial species [102, 106]. Compared to unexposed monocytic cells, tobacco-exposure suppresses general responsiveness to bacteria and lipopolysaccharide (LPS) [108], reflected in a down-regulation of surface pathogen recognition receptors (TLR-2 and MARCO) [109, 110]; with reduced phagocytic, reactive-oxygen species generating, and bacterial killing capacities also reported [105, 106, 111]. Dendritic cells, whose primary function is to process antigen and present them to adaptive immune cells thus bridging innate and adapative immune responses, are also negatively influenced by tobacco smoke and smoke constituents. For example, nicotine exposure suppresses the maturation dendritic cells that, subsequently, exhibit a reduced expression of antigen presenting and costimulatory molecules (MHC Class II, CD80 and CD86), reduced capacity for antigen uptake and reduced production of T cell stimulating cytokines in response to the archetypal Gram-negative pro-inflammatory stimulus, LPS [112, 113].

Dysregulation of adaptive immune function

The potential effects of smoking on lymphocyte function are not well understood. However, while IgE levels are increased in smokers compared to non-smokers, concentrations of anti-bacterial IgG levels are reduced [114118]. This may represent a key underlying mechanism of increased susceptibility to bacterial infection in smokers. Furthermore, in order to mount a successful humoral immune response, B cells require T helper cell-derived cytokines to proliferate and differentiate into plasma cells and to promote immunoglobulin class switching. However, it has been shown by several groups that tobacco smoke reduces T cell proliferative responses to mitogen/antigen [119121], with similar tobacco-induced reductions in B cell proliferative responses also reported [122]. For further details of the influence of tobacco smoke on the immune system, we point the reader to several extensive reviews [54, 69, 71, 123129].

Summary

The available evidence supporting tobacco smoke as a risk factor for multiple and varied bacterial infections is convincing. A summary of bacterial infections associated with tobacco smoking [2, 4, 5, 22, 28, 38, 44, 51, 130138] is presented in Table 1. Additional references are provided for more complete information (nasopharyngeal and respiratory pathogens [13, 5, 6, 9, 13, 14]; Group A streptococcus [15]; Legionnaires disease [5, 23]; cystic fibrosis [17, 18]; pneumonia [2, 20, 21]; tuberculosis [3033]; meningococcal carriage [4, 3437, 39, 139]; bacterial vaginosis [43, 45, 46]; periductal mastitis [140, 141]; Helicobacter pylori [49, 50, 52, 53]; periodontitis [54, 123, 142151]; ulcerative colitis [71, 152, 153]; Crohn's disease [152, 154, 155]; otitis media [1, 73, 156]; and surgical infections [75, 76, 80]).
Table 1

Bacterial infections associated with tobacco smoking.

Infection

OR (95% CI)*

Nasopharyngeal and respiratory pathogens (such as S. pneumonia, N. meningitidis, H. influenzae, L. pneumophila)

2.5 (1.1–6.0) [4]

Group A streptococcus sore throat

-

Legionnaires disease

3.6 (2.1–5.8) [5]

Cystic fibrosis

Increased severity on smoke exposure[134, 138]

Pneumonia

2.6 (1.9–3.5)[22, 137]

Tuberculosis

1.8 Light [29]

 

3.2 Moderate [29]

 

3.7 Heavy [29]

 

4.1 (2.4 to 7.3) Active [2]

 

2.5 (1.2 to 5.1) Secondhand [2]

Meningococcal carriage

2.2 (1.0–4.8) Light [38]

 

7.2 (2.3–22.9 Heavy [38]

Bacterial vaginosis

2.7 [44]

Periductal mastitis

6.2 (2.9–13.4) [131]

Helicobacter pylori

1.9 (1.4–2.5) [51]

Periodontitis

3.3 (2.3–4.5) Light [132]

 

7.3 (5.1–10.3) Heavy [132]

Ulcerative colitis

0.6 (0.4–0.8) [70]

Crohn's disease

3.6 (2.5 – 5.0) Active [130]

 

2.0 (1.3 – 3.3) Secondhand [135]

Otitis media

4.2 (1.5–11.9) Secondhand [133]

Surgical infections

1.2 (1.1, 1.3) [136]

* The specific OR (95% CI) presented is selected from a single reference/study. Additional references are provided in the text for more complete information.

Nevertheless, there are several limitations to many individual studies. For example, some studies have small subject numbers. Others have found associations between tobacco smoke exposure and infection during in studies designed to answer different specific questions. Importantly, many additional factors are independently associated with bacterial infection, including age, socioeconomic status, healthcare provision, alcohol, low physical activity, certain sexual behaviors, and not all studies reporting on the associations between smoking and infection have addressed all confounders.

It is also important to note that in the existing literature on mechanisms of tobacco-induced disease, there is an overbearing focus on nicotine. While this approach is valid, it must be remembered that tobacco smoke contains more than 4000 chemicals and there is an urgent need for studies that examine other components of cigarette smoke as well as whole mainstream and side stream smoke preparations. To this end, there remains a pressing need for consensus on the standardization of in vivo and in vitro modeling systems to permit the generation of a more robust and reproducible evidence base.

We hope that this review will serve to generate a wider understanding of the increased susceptibility to infectious diseases in smoke-exposed individuals; provide further impetus to efforts aimed at reducing smoke exposure; and act as a stimulus for further epidemiological and, particularly, mechanistic research into this important area.

Declarations

Authors’ Affiliations

(1)
Department of Microbiology and Immunology, University of Louisville
(2)
Department of Pharmacology and Toxicology, University of Louisville
(3)
Oral Health and Systemic Disease Research Group, University of Louisville

References

  1. Murphy TF: Otitis media, bacterial colonization, and the smoking parent. Clin Infect Dis. 2006, 42 (7): 904-906. 10.1086/500942.PubMedGoogle Scholar
  2. Nuorti JP, Butler JC, Farley MM, Harrison LH, McGeer A, Kolczak MS, Breiman RF: Cigarette smoking and invasive pneumococcal disease. Active Bacterial Core Surveillance Team. N Engl J Med. 2000, 342 (10): 681-689. 10.1056/NEJM200003093421002.PubMedGoogle Scholar
  3. Fischer M, Hedberg K, Cardosi P, Plikaytis BD, Hoesly FC, Steingart KR, Bell TA, Fleming DW, Wenger JD, Perkins BA: Tobacco smoke as a risk factor for meningococcal disease. Pediatr Infect Dis J. 1997, 16 (10): 979-983. 10.1097/00006454-199710000-00015.PubMedGoogle Scholar
  4. Iles K, Poplawski NK, Couper RT: Passive exposure to tobacco smoke and bacterial meningitis in children. J Paediatr Child Health. 2001, 37 (4): 388-391. 10.1046/j.1440-1754.2001.00698.x.PubMedGoogle Scholar
  5. Straus WL, Plouffe JF, File TM, Lipman HB, Hackman BH, Salstrom SJ, Benson RF, Breiman RF: Risk factors for domestic acquisition of legionnaires disease. Ohio legionnaires Disease Group. Arch Intern Med. 1996, 156 (15): 1685-1692. 10.1001/archinte.156.15.1685.PubMedGoogle Scholar
  6. Brook I, Gober AE: Recovery of potential pathogens and interfering bacteria in the nasopharynx of smokers and nonsmokers. Chest. 2005, 127 (6): 2072-2075. 10.1378/chest.127.6.2072.PubMedGoogle Scholar
  7. El Ahmer OR, Essery SD, Saadi AT, Raza MW, Ogilvie MM, Weir DM, Blackwell CC: The effect of cigarette smoke on adherence of respiratory pathogens to buccal epithelial cells. FEMS Immunol Med Microbiol. 1999, 23 (1): 27-36.PubMedGoogle Scholar
  8. Fujimori I, Goto R, Kikushima K, Ogino J, Hisamatsu K, Murakami Y, Yamada T: [Isolation of alpha-streptococci with inhibitory activity against pathogens, in the oral cavity and the effect of tobacco and gargling on oral flora]. Kansenshogaku Zasshi. 1995, 69 (2): 133-138.PubMedGoogle Scholar
  9. Brook I, Gober AE: Effect of smoking cessation on the microbial flora. Arch Otolaryngol Head Neck Surg. 2007, 133 (2): 135-138. 10.1001/archotol.133.2.135.PubMedGoogle Scholar
  10. Zalacain R, Sobradillo V, Amilibia J, Barron J, Achotegui V, Pijoan JI, Llorente JL: Predisposing factors to bacterial colonization in chronic obstructive pulmonary disease. Eur Respir J. 1999, 13 (2): 343-348. 10.1034/j.1399-3003.1999.13b21.x.PubMedGoogle Scholar
  11. Monso E, Garcia-Aymerich J, Soler N, Farrero E, Felez MA, Anto JM, Torres A: Bacterial infection in exacerbated COPD with changes in sputum characteristics. Epidemiol Infect. 2003, 131 (1): 799-804. 10.1017/S0950268803008872.PubMed CentralPubMedGoogle Scholar
  12. Tumkaya M, Atis S, Ozge C, Delialioglu N, Polat G, Kanik A: Relationship between airway colonization, inflammation and exacerbation frequency in COPD. Respir Med. 2007, 101 (4): 729-737. 10.1016/j.rmed.2006.08.020.PubMedGoogle Scholar
  13. Segala C, Poizeau D, Neukirch F, Aubier M, Samson J, Gehanno P: Air pollution, passive smoking, and respiratory symptoms in adults. Arch Environ Health. 2004, 59 (12): 669-676.PubMedGoogle Scholar
  14. Wakefield M, Trotter L, Cameron M, Woodward A, Inglis G, Hill D: Association between exposure to workplace secondhand smoke and reported respiratory and sensory symptoms: cross-sectional study. J Occup Environ Med. 2003, 45 (6): 622-627. 10.1097/01.jom.0000069242.06498.86.PubMedGoogle Scholar
  15. Nandi S, Kumar R, Ray P, Vohra H, Ganguly NK: Group A streptococcal sore throat in a periurban population of northern India: a one-year prospective study. Bull World Health Organ. 2001, 79 (6): 528-533.PubMed CentralPubMedGoogle Scholar
  16. Gomez MI, Prince A: Opportunistic infections in lung disease: Pseudomonas infections in cystic fibrosis. Curr Opin Pharmacol. 2007, 7 (3): 244-251. 10.1016/j.coph.2006.12.005.PubMedGoogle Scholar
  17. Collaco JM, Vanscoy L, Bremer L, McDougal K, Blackman SM, Bowers A, Naughton K, Jennings J, Ellen J, Cutting GR: Interactions between secondhand smoke and genes that affect cystic fibrosis lung disease. JAMA. 2008, 299 (4): 417-424. 10.1001/jama.299.4.417.PubMed CentralPubMedGoogle Scholar
  18. Verma A, Clough D, McKenna D, Dodd M, Webb AK: Smoking and cystic fibrosis. J R Soc Med. 2001, 94 (Suppl 40): 29-34.PubMed CentralPubMedGoogle Scholar
  19. Drannik AG, Pouladi MA, Robbins CS, Goncharova SI, Kianpour S, Stampfli MR: Impact of cigarette smoke on clearance and inflammation after Pseudomonas aeruginosa infection. Am J Respir Crit Care Med. 2004, 170 (11): 1164-1171. 10.1164/rccm.200311-1521OC.PubMedGoogle Scholar
  20. Bansal S, Kashyap S, Pal LS, Goel A: Clinical and bacteriological profile of community acquired pneumonia in Shimla, Himachal Pradesh. Indian J Chest Dis Allied Sci. 2004, 46 (1): 17-22.PubMedGoogle Scholar
  21. Greene CM, Kyaw MH, Ray SM, Schaffner W, Lynfield R, Barrett NL, Long C, Gershman K, Pilishvili T, Roberson A, et al: Preventability of invasive pneumococcal disease and assessment of current polysaccharide vaccine recommendations for adults: United States, 2001–2003. Clin Infect Dis. 2006, 43 (2): 141-150. 10.1086/505117.PubMedGoogle Scholar
  22. Arcavi L, Benowitz NL: Cigarette smoking and infection. Arch Intern Med. 2004, 164 (20): 2206-2216. 10.1001/archinte.164.20.2206.PubMedGoogle Scholar
  23. Doebbeling BN, Wenzel RP: The epidemiology of Legionella pneumophila infections. Semin Respir Infect. 1987, 2 (4): 206-221.PubMedGoogle Scholar
  24. Poupard M, Campese C, Bernillon P, Che D: [Factors associated with mortality in Legionnaires' disease, France, 2002–2004]. Med Mal Infect. 2007, 37 (6): 325-330.PubMedGoogle Scholar
  25. Ricketts KD, Joseph CA: Legionnaires' disease in Europe 2003–2004. Euro Surveill. 2005, 10 (12): 256-259.PubMedGoogle Scholar
  26. Wang SP, Wang JS, Li HF: [A study on the risk factors of Legionella infection in children]. Zhonghua Liu Xing Bing Xue Za Zhi. 1995, 16 (2): 88-91.PubMedGoogle Scholar
  27. Che D, Campese C, Santa-Olalla P, Jacquier G, Bitar D, Bernillon P, Desenclos JC: Sporadic community-acquired Legionnaires' disease in France: a 2-year national matched case-control study. Epidemiol Infect. 2008, 136 (12): 1684-1690. 10.1017/S0950268807000283.PubMed CentralPubMedGoogle Scholar
  28. WHO: The world health report 1999 – making a difference. 1999Google Scholar
  29. Kolappan C, Gopi PG: Tobacco smoking and pulmonary tuberculosis. Thorax. 2002, 57 (11): 964-966. 10.1136/thorax.57.11.964.PubMed CentralPubMedGoogle Scholar
  30. Kolappan C, Gopi PG, Subramani R, Narayanan PR: Selected biological and behavioural risk factors associated with pulmonary tuberculosis. Int J Tuberc Lung Dis. 2007, 11 (9): 999-1003.PubMedGoogle Scholar
  31. Altet-Gomez MN, Alcaide J, Godoy P, Romero MA, Hernandez del Rey I: Clinical and epidemiological aspects of smoking and tuberculosis: a study of 13,038 cases. Int J Tuberc Lung Dis. 2005, 9 (4): 430-436.PubMedGoogle Scholar
  32. Chiang CY, Slama K, Enarson DA: Associations between tobacco and tuberculosis. Int J Tuberc Lung Dis. 2007, 11 (3): 258-262.PubMedGoogle Scholar
  33. Slama K, Chiang CY, Enarson DA, Hassmiller K, Fanning A, Gupta P, Ray C: Tobacco and tuberculosis: a qualitative systematic review and meta-analysis. Int J Tuberc Lung Dis. 2007, 11 (10): 1049-1061.PubMedGoogle Scholar
  34. Gold R: Epidemiology of bacterial meningitis. Infect Dis Clin North Am. 1999, 13 (3): 515-525. 10.1016/S0891-5520(05)70092-1.PubMedGoogle Scholar
  35. Stanwell-Smith RE, Stuart JM, Hughes AO, Robinson P, Griffin MB, Cartwright K: Smoking, the environment and meningococcal disease: a case control study. Epidemiol Infect. 1994, 112 (2): 315-328.PubMed CentralPubMedGoogle Scholar
  36. Stuart JM, Cartwright KA, Dawson JA, Rickard J, Noah ND: Risk factors for meningococcal disease: a case control study in south west England. Community Med. 1988, 10 (2): 139-146.PubMedGoogle Scholar
  37. Tappero JW, Reporter R, Wenger JD, Ward BA, Reeves MW, Missbach TS, Plikaytis BD, Mascola L, Schuchat A: Meningococcal disease in Los Angeles County, California, and among men in the county jails. N Engl J Med. 1996, 335 (12): 833-840. 10.1056/NEJM199609193351201.PubMedGoogle Scholar
  38. Riordan T, Cartwright K, Andrews N, Stuart J, Burris A, Fox A, Borrow R, Douglas-Riley T, Gabb J, Miller A: Acquisition and carriage of meningococci in marine commando recruits. Epidemiol Infect. 1998, 121 (3): 495-505. 10.1017/S0950268898001496.PubMed CentralPubMedGoogle Scholar
  39. Melles DC, Bogaert D, Gorkink RF, Peeters JK, Moorhouse MJ, Ott A, van Leeuwen WB, Simons G, Verbrugh HA, Hermans PW, et al: Nasopharyngeal co-colonization with Staphylococcus aureus and Streptococcus pneumoniae in children is bacterial genotype independent. Microbiology. 2007, 153 (Pt 3): 686-692. 10.1099/mic.0.2006/002279-0.PubMedGoogle Scholar
  40. Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J: Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ. 1994, 308 (6924): 295-298.PubMed CentralPubMedGoogle Scholar
  41. Oakeshott P, Hay P, Hay S, Steinke F, Rink E, Kerry S: Association between bacterial vaginosis or chlamydial infection and miscarriage before 16 weeks' gestation: prospective community based cohort study. BMJ. 2002, 325 (7376): 1334-10.1136/bmj.325.7376.1334.PubMed CentralPubMedGoogle Scholar
  42. Koumans EH, Sternberg M, Bruce C, McQuillan G, Kendrick J, Sutton M, Markowitz LE: The prevalence of bacterial vaginosis in the United States, 2001–2004; associations with symptoms, sexual behaviors, and reproductive health. Sex Transm Dis. 2007, 34 (11): 864-869. 10.1097/OLQ.0b013e318074e565.PubMedGoogle Scholar
  43. Larsson PG, Fahraeus L, Carlsson B, Jakobsson T, Forsum U: Predisposing factors for bacterial vaginosis, treatment efficacy and pregnancy outcome among term deliveries; results from a preterm delivery study. BMC Womens Health. 2007, 7: 20-10.1186/1472-6874-7-20.PubMed CentralPubMedGoogle Scholar
  44. Evans AL, Scally AJ, Wellard SJ, Wilson JD: Prevalence of bacterial vaginosis in lesbians and heterosexual women in a community setting. Sex Transm Infect. 2007, 83 (6): 470-475. 10.1136/sti.2006.022277.PubMed CentralPubMedGoogle Scholar
  45. Nelson DB, Bellamy S, Odibo A, Nachamkin I, Ness RB, Allen-Taylor L: Vaginal symptoms and bacterial vaginosis (BV): how useful is self-report? Development of a screening tool for predicting BV status. Epidemiol Infect. 2007, 135 (8): 1369-1375. 10.1017/S095026880700787X.PubMed CentralPubMedGoogle Scholar
  46. Miller GC, McDermott R, McCulloch B, Fairley CK, Muller R: Predictors of the prevalence of bacterial STI among young disadvantaged Indigenous people in north Queensland, Australia. Sex Transm Infect. 2003, 79 (4): 332-335. 10.1136/sti.79.4.332.PubMed CentralPubMedGoogle Scholar
  47. Maity P, Biswas K, Roy S, Banerjee RK, Bandyopadhyay U: Smoking and the pathogenesis of gastroduodenal ulcer – recent mechanistic update. Mol Cell Biochem. 2003, 253 (1–2): 329-338. 10.1023/A:1026040723669.PubMedGoogle Scholar
  48. Ainsworth MA, Hogan DL, Koss MA, Isenberg JI: Cigarette smoking inhibits acid-stimulated duodenal mucosal bicarbonate secretion. Ann Intern Med. 1993, 119 (9): 882-886.PubMedGoogle Scholar
  49. Regula J, Hennig E, Burzykowski T, Orlowska J, Przytulski K, Polkowski M, Dziurkowska-Marek A, Marek T, Nowak A, Butruk E, et al: Multivariate analysis of risk factors for development of duodenal ulcer in Helicobacter pylori-infected patients. Digestion. 2003, 67 (1–2): 25-31. 10.1159/000070394.PubMedGoogle Scholar
  50. Menzel M, Hogel J, Allmendinger G, Schmid E: Relative risks of age, gender, nationality, smoking, and Helicobacter-pylori-infection in duodenal and gastric ulcer and interactions. Z Gastroenterol. 1995, 33 (4): 193-197.PubMedGoogle Scholar
  51. Cardenas VM, Graham DY: Smoking and Helicobacter pylori infection in a sample of U.S. adults. Epidemiology. 2005, 16 (4): 586-590. 10.1097/01.ede.0000165365.52904.4a.PubMedGoogle Scholar
  52. De Francesco V, Zullo A, Margiotta M, Marangi S, Burattini O, Berloco P, Russo F, Barone M, Di Leo A, Minenna MF, et al: Sequential treatment for Helicobacter pylori does not share the risk factors of triple therapy failure. Aliment Pharmacol Ther. 2004, 19 (4): 407-414. 10.1046/j.1365-2036.2004.01818.x.PubMedGoogle Scholar
  53. Suzuki T, Matsuo K, Ito H, Sawaki A, Hirose K, Wakai K, Sato S, Nakamura T, Yamao K, Ueda R, et al: Smoking increases the treatment failure for Helicobacter pylori eradication. Am J Med. 2006, 119 (3): 217-224. 10.1016/j.amjmed.2005.10.003.PubMedGoogle Scholar
  54. Palmer RM, Wilson RF, Hasan AS, Scott DA: Mechanisms of action of environmental factors – tobacco smoking. J Clin Periodontol. 2005, 32 (Suppl 6): 180-195. 10.1111/j.1600-051X.2005.00786.x.PubMedGoogle Scholar
  55. Bostrom L, Bergstrom J, Dahlen G, Linder LE: Smoking and subgingival microflora in periodontal disease. J Clin Periodontol. 2001, 28 (3): 212-219. 10.1034/j.1600-051x.2001.028003212.x.PubMedGoogle Scholar
  56. Darby IB, Hodge PJ, Riggio MP, Kinane DF: Clinical and microbiological effect of scaling and root planing in smoker and non-smoker chronic and aggressive periodontitis patients. J Clin Periodontol. 2005, 32 (2): 200-206. 10.1111/j.1600-051X.2005.00644.x.PubMedGoogle Scholar
  57. Preber H, Bergstrom J, Linder LE: Occurrence of periopathogens in smoker and non-smoker patients. J Clin Periodontol. 1992, 19 (9 Pt 1): 667-671. 10.1111/j.1600-051X.1992.tb01716.x.PubMedGoogle Scholar
  58. Stoltenberg JL, Osborn JB, Pihlstrom BL, Herzberg MC, Aeppli DM, Wolff LF, Fischer GE: Association between cigarette smoking, bacterial pathogens, and periodontal status. J Periodontol. 1993, 64 (12): 1225-1230.PubMedGoogle Scholar
  59. Zambon JJ, Grossi SG, Machtei EE, Ho AW, Dunford R, Genco RJ: Cigarette smoking increases the risk for subgingival infection with periodontal pathogens. J Periodontol. 1996, 67 (10 Suppl): 1050-1054.PubMedGoogle Scholar
  60. Haffajee AD, Socransky SS: Relationship of cigarette smoking to the subgingival microbiota. J Clin Periodontol. 2001, 28 (5): 377-388. 10.1034/j.1600-051x.2001.028005377.x.PubMedGoogle Scholar
  61. Kamma JJ, Nakou M, Baehni PC: Clinical and microbiological characteristics of smokers with early onset periodontitis. J Periodontal Res. 1999, 34 (1): 25-33. 10.1111/j.1600-0765.1999.tb02218.x.PubMedGoogle Scholar
  62. Eggert FM, McLeod MH, Flowerdew G: Effects of smoking and treatment status on periodontal bacteria: evidence that smoking influences control of periodontal bacteria at the mucosal surface of the gingival crevice. J Periodontol. 2001, 72 (9): 1210-1220. 10.1902/jop.2000.72.9.1210.PubMedGoogle Scholar
  63. Umeda M, Chen C, Bakker I, Contreras A, Morrison JL, Slots J: Risk indicators for harboring periodontal pathogens. J Periodontol. 1998, 69 (10): 1111-1118.PubMedGoogle Scholar
  64. van Winkelhoff AJ, Bosch-Tijhof CJ, Winkel EG, Reijden van der WA: Smoking affects the subgingival microflora in periodontitis. J Periodontol. 2001, 72 (5): 666-671. 10.1902/jop.2001.72.5.666.PubMedGoogle Scholar
  65. Shiloah J, Patters MR, Waring MB: The prevalence of pathogenic periodontal microflora in healthy young adult smokers. J Periodontol. 2000, 71 (4): 562-567. 10.1902/jop.2000.71.4.562.PubMedGoogle Scholar
  66. Gomes SC, Piccinin FB, Oppermann RV, Susin C, Nonnenmacher CI, Mutters R, Marcantonio RA: Periodontal status in smokers and never-smokers: clinical findings and real-time polymerase chain reaction quantification of putative periodontal pathogens. J Periodontol. 2006, 77 (9): 1483-1490. 10.1902/jop.2006.060026.PubMedGoogle Scholar
  67. Socransky SS, Haffajee AD: Periodontal microbial ecology. Periodontol 2000. 2005, 38: 135-187. 10.1111/j.1600-0757.2005.00107.x.PubMedGoogle Scholar
  68. Danese S, Sans M, Fiocchi C: Inflammatory bowel disease: the role of environmental factors. Autoimmun Rev. 2004, 3 (5): 394-400. 10.1016/j.autrev.2004.03.002.PubMedGoogle Scholar
  69. Scott DA, Martin M: Exploitation of the nicotinic anti-inflammatory pathway for the treatment of epithelial inflammatory diseases. World J Gastroenterol. 2006, 12 (46): 7451-7459.PubMed CentralPubMedGoogle Scholar
  70. Mahid SS, Minor KS, Soto RE, Hornung CA, Galandiuk S: Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc. 2006, 81 (11): 1462-1471.PubMedGoogle Scholar
  71. Lakatos PL, Szamosi T, Lakatos L: Smoking in inflammatory bowel diseases: good, bad or ugly?. World J Gastroenterol. 2007, 13 (46): 6134-6139. 10.3748/wjg.13.6134.PubMed CentralPubMedGoogle Scholar
  72. Hanauer SB: Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis. 2006, 12 (Suppl 1): S3-9. 10.1097/01.MIB.0000195385.19268.68.PubMedGoogle Scholar
  73. Brook I, Gober AE: Recovery of potential pathogens and interfering bacteria in the nasopharynx of otitis media-prone children and their smoking and nonsmoking parents. Arch Otolaryngol Head Neck Surg. 2005, 131 (6): 509-512. 10.1001/archotol.131.6.509.PubMedGoogle Scholar
  74. CDC: Secondhand Smoke and Children. 2008Google Scholar
  75. Cheadle WG: Risk factors for surgical site infection. Surg Infect (Larchmt). 2006, 7 (Suppl 1): S7-11.Google Scholar
  76. Haas JP, Evans AM, Preston KE, Larson EL: Risk factors for surgical site infection after cardiac surgery: the role of endogenous flora. Heart Lung. 2005, 34 (2): 108-114. 10.1016/j.hrtlng.2004.02.004.PubMedGoogle Scholar
  77. Saint S, Kaufman SR, Rogers MA, Baker PD, Boyko EJ, Lipsky BA: Risk factors for nosocomial urinary tract-related bacteremia: a case-control study. Am J Infect Control. 2006, 34 (7): 401-407. 10.1016/j.ajic.2006.03.001.PubMedGoogle Scholar
  78. Huttunen R, Laine J, Lumio J, Vuento R, Syrjanen J: Obesity and smoking are factors associated with poor prognosis in patients with bacteraemia. BMC Infect Dis. 2007, 7: 13-10.1186/1471-2334-7-13.PubMed CentralPubMedGoogle Scholar
  79. Kelsey MC, Mitchell CA, Griffin M, Spencer RC, Emmerson AM: Prevalence of lower respiratory tract infections in hospitalized patients in the United Kingdom and Eire – results from the Second National Prevalence Survey. J Hosp Infect. 2000, 46 (1): 12-22. 10.1053/jhin.2000.0775.PubMedGoogle Scholar
  80. Luksamijarulkul P, Parikumsil N, Poomsuwan V, Konkeaw W: Nosocomial surgical site infection among Photharam Hospital patients with surgery: incidence, risk factors and development of risk screening form. J Med Assoc Thai. 2006, 89 (1): 81-89.PubMedGoogle Scholar
  81. Mathews TJ: Smoking during pregnancy in the 1990s. Natl Vital Stat Rep. 2001, 49 (7): 1-14.Google Scholar
  82. Kum-Nji P, Meloy L, Herrod HG: Environmental tobacco smoke exposure: prevalence and mechanisms of causation of infections in children. Pediatrics. 2006, 117 (5): 1745-1754. 10.1542/peds.2005-1886.PubMedGoogle Scholar
  83. Yolton K, Dietrich K, Auinger P, Lanphear BP, Hornung R: Exposure to environmental tobacco smoke and cognitive abilities among U.S. children and adolescents. Environ Health Perspect. 2005, 113 (1): 98-103.PubMed CentralPubMedGoogle Scholar
  84. Noakes P, Taylor A, Hale J, Breckler L, Richmond P, Devadason SG, Prescott SL: The effects of maternal smoking on early mucosal immunity and sensitization at 12 months of age. Pediatr Allergy Immunol. 2007, 18 (2): 118-127. 10.1111/j.1399-3038.2006.00490.x.PubMedGoogle Scholar
  85. Jeppesen DL, Nielsen SD, Ersboll AK, Valerius NH: Maternal Smoking during Pregnancy Increases the Risk of Postnatal Infections in Preterm Neonates. Neonatology. 2008, 94 (2): 75-78. 10.1159/000113535.PubMedGoogle Scholar
  86. Sayers NM, Drucker DB: Animal models used to test the interactions between infectious agents and products of cigarette smoked implicated in sudden infant death syndrome. FEMS Immunol Med Microbiol. 1999, 25 (1–2): 115-123. 10.1111/j.1574-695X.1999.tb01334.x.PubMedGoogle Scholar
  87. Sayers NM, Drucker DB, Telford DR, Morris JA: Effects of nicotine on bacterial toxins associated with cot death. Arch Dis Child. 1995, 73 (6): 549-551. 10.1136/adc.73.6.549.PubMed CentralPubMedGoogle Scholar
  88. Prandota J: Possible pathomechanisms of sudden infant death syndrome: key role of chronic hypoxia, infection/inflammation states, cytokine irregularities, and metabolic trauma in genetically predisposed infants. Am J Ther. 2004, 11 (6): 517-546. 10.1097/01.mjt.0000140648.30948.bd.PubMedGoogle Scholar
  89. Scott DA, Wang XL: Molecular Mechanisms of Tobacco-Induced Diseases. 2006Google Scholar
  90. Gensch E, Gallup M, Sucher A, Li D, Gebremichael A, Lemjabbar H, Mengistab A, Dasari V, Hotchkiss J, Harkema J, et al: Tobacco smoke control of mucin production in lung cells requires oxygen radicals AP-1 and JNK. J Biol Chem. 2004, 279 (37): 39085-39093. 10.1074/jbc.M406866200.PubMedGoogle Scholar
  91. Hodge S, Hodge G, Ahern J, Jersmann H, Holmes M, Reynolds PN: Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2007, 37 (6): 748-755. 10.1165/rcmb.2007-0025OC.PubMedGoogle Scholar
  92. Akishima S, Matsushita S, Sato F, Hyodo K, Imazuru T, Enomoto Y, Noma M, Hiramatsu Y, Shigeta O, Sakakibara Y: Cigarette-smoke-induced vasoconstriction of peripheral arteries: evaluation by synchrotron radiation microangiography. Circ J. 2007, 71 (3): 418-422. 10.1253/circj.71.418.PubMedGoogle Scholar
  93. Bernardi L, Casucci G, Haider T, Brandstatter E, Pocecco E, Ehrenbourg I, Burtscher M: Autonomic and cerebro-vascular abnormalities in mild copd are worsened by chronic smoking. Eur Respir J. 2008Google Scholar
  94. Meekin TN, Wilson RF, Scott DA, Ide M, Palmer RM: Laser Doppler flowmeter measurement of relative gingival and forehead skin blood flow in light and heavy smokers during and after smoking. J Clin Periodontol. 2000, 27 (4): 236-242. 10.1034/j.1600-051x.2000.027004236.x.PubMedGoogle Scholar
  95. Rezavandi K, Palmer RM, Odell EW, Scott DA, Wilson RF: Expression of ICAM-1 and E-selectin in gingival tissues of smokers and non-smokers with periodontitis. J Oral Pathol Med. 2002, 31 (1): 59-64.PubMedGoogle Scholar
  96. Nair P, Sutherland G, Palmer RM, Wilson RF, Scott DA: Gingival bleeding on probing increases after quitting smoking. J Clin Periodontol. 2003, 30 (5): 435-437. 10.1034/j.1600-051X.2003.20039.x.PubMedGoogle Scholar
  97. Wiedeman JA, Kaul R, Heuer LS, Thao NN, Pinkerton KE, Wenman WM: Tobacco smoke induces persistent infection of Chlamydophila pneumoniae in HEp-2 cells. Microb Pathog. 2004, 37 (3): 141-148. 10.1016/j.micpath.2004.06.006.PubMedGoogle Scholar
  98. Wiedeman JA, Kaul R, Heuer LS, Thao NN, Pinkerton KE, Wenman WM: Tobacco smoke induces a persistent, but recoverable state in Chlamydia pneumoniae infection of human endothelial cells. Microb Pathog. 2005, 39 (5–6): 197-204.PubMedGoogle Scholar
  99. Zonuz AT, Rahmati A, Mortazavi H, Khashabi E, Farahani RM: Effect of cigarette smoke exposure on the growth of Streptococcus mutans and Streptococcus sanguis: an in vitro study. Nicotine Tob Res. 2008, 10 (1): 63-67. 10.1080/14622200701705035.PubMedGoogle Scholar
  100. Ertel A, Eng R, Smith SM: The differential effect of cigarette smoke on the growth of bacteria found in humans. Chest. 1991, 100 (3): 628-630. 10.1378/chest.100.3.628.PubMedGoogle Scholar
  101. Pavlova SI, Tao L: Induction of vaginal Lactobacillus phages by the cigarette smoke chemical benzo[a]pyrene diol epoxide. Mutat Res. 2000, 466 (1): 57-62.PubMedGoogle Scholar
  102. Xu M, Scott JE, Liu KZ, Bishop HR, Renaud DE, Palmer RM, Soussi-Gounni A, Scott DA: The influence of nicotine on granulocytic differentiation – inhibition of the oxidative burst and bacterial killing and increased matrix metalloproteinase-9 release. BMC Cell Biol. 2008, 9 (1): 19-10.1186/1471-2121-9-19.PubMed CentralPubMedGoogle Scholar
  103. Zappacosta B, Persichilli S, Minucci A, Stasio ED, Carlino P, Pagliari G, Giardina B, Sole PD: Effect of aqueous cigarette smoke extract on the chemiluminescence kinetics of polymorphonuclear leukocytes and on their glycolytic and phagocytic activity. Luminescence. 2001, 16 (5): 315-319. 10.1002/bio.661.PubMedGoogle Scholar
  104. Stringer KA, Tobias M, O'Neill HC, Franklin CC: Cigarette smoke extract-induced suppression of caspase-3-like activity impairs human neutrophil phagocytosis. Am J Physiol Lung Cell Mol Physiol. 2007, 292 (6): L1572-1579. 10.1152/ajplung.00325.2006.PubMedGoogle Scholar
  105. Sorensen LT, Nielsen HB, Kharazmi A, Gottrup F: Effect of smoking and abstention on oxidative burst and reactivity of neutrophils and monocytes. Surgery. 2004, 136 (5): 1047-1053. 10.1016/j.surg.2004.04.001.PubMedGoogle Scholar
  106. Pabst MJ, Pabst KM, Collier JA, Coleman TC, Lemons-Prince ML, Godat MS, Waring MB, Babu JP: Inhibition of neutrophil and monocyte defensive functions by nicotine. J Periodontol. 1995, 66 (12): 1047-1055.PubMedGoogle Scholar
  107. Dunn JS, Freed BM, Gustafson DL, Stringer KA: Inhibition of human neutrophil reactive oxygen species production and p67phox translocation by cigarette smoke extract. Atherosclerosis. 2005, 179 (2): 261-267. 10.1016/j.atherosclerosis.2004.11.011.PubMedGoogle Scholar
  108. McMaster SK, Paul-Clark MJ, Walters M, Fleet M, Anandarajah J, Sriskandan S, Mitchell JA: Cigarette smoke inhibits macrophage sensing of Gram-negative bacteria and lipopolysaccharide: relative roles of nicotine and oxidant stress. Br J Pharmacol. 2008, 153 (3): 536-543. 10.1038/sj.bjp.0707595.PubMed CentralPubMedGoogle Scholar
  109. Versteeg D, Dol E, Hoefer IE, Flier S, Buhre WF, de Kleijn D, van Dongen EP, Pasterkamp G, de Vries JP: Toll-Like Receptor 2 and 4 Response and Expression on Monocytes Decrease Rapidly in Patients Undergoing Arterial Surgery and Are Related to Preoperative Smoking. Shock. 2008, 31 (1): 21-27. 10.1097/SHK.0b013e31817d43bf.Google Scholar
  110. Baqir M, Chen CZ, Martin RJ, Thaikoottathil J, Case SR, Minor MN, Bowler R, Chu HW: Cigarette smoke decreases MARCO expression in macrophages: Implication in Mycoplasma pneumoniae infection. Respir Med. 2008Google Scholar
  111. King TE, Savici D, Campbell PA: Phagocytosis and killing of Listeria monocytogenes by alveolar macrophages: smokers versus nonsmokers. J Infect Dis. 1988, 158 (6): 1309-1316.PubMedGoogle Scholar
  112. Nouri-Shirazi M, Tinajero R, Guinet E: Nicotine alters the biological activities of developing mouse bone marrow-derived dendritic cells (DCs). Immunol Lett. 2007, 109 (2): 155-164. 10.1016/j.imlet.2007.02.005.PubMedGoogle Scholar
  113. Robbins CS, Franco F, Mouded M, Cernadas M, Shapiro SD: Cigarette smoke exposure impairs dendritic cell maturation and T cell proliferation in thoracic lymph nodes of mice. J Immunol. 2008, 180 (10): 6623-6628.PubMed CentralPubMedGoogle Scholar
  114. Quinn SM, Zhang JB, Gunsolley JC, Schenkein HA, Tew JG: The influence of smoking and race on adult periodontitis and serum IgG2 levels. J Periodontol. 1998, 69 (2): 171-177.PubMedGoogle Scholar
  115. Quinn SM, Zhang JB, Gunsolley JC, Schenkein JG, Schenkein HA, Tew JG: Influence of smoking and race on immunoglobulin G subclass concentrations in early-onset periodontitis patients. Infect Immun. 1996, 64 (7): 2500-2505.PubMed CentralPubMedGoogle Scholar
  116. Gonzalez-Quintela A, Alende R, Gude F, Campos J, Rey J, Meijide LM, Fernandez-Merino C, Vidal C: Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin Exp Immunol. 2008, 151 (1): 42-50.PubMed CentralPubMedGoogle Scholar
  117. Gunsolley JC, Pandey JP, Quinn SM, Tew J, Schenkein HA: The effect of race, smoking and immunoglobulin allotypes on IgG subclass concentrations. J Periodontal Res. 1997, 32 (4): 381-387. 10.1111/j.1600-0765.1997.tb00548.x.PubMedGoogle Scholar
  118. Miyake Y, Miyamoto S, Ohya Y, Sasaki S, Matsunaga I, Yoshida T, Hirota Y, Oda H: Relationship between active and passive smoking and total serum IgE levels in Japanese women: baseline data from the Osaka Maternal and Child Health Study. Int Arch Allergy Immunol. 2004, 135 (3): 221-228. 10.1159/000081307.PubMedGoogle Scholar
  119. Thatcher TH, Benson RP, Phipps RP, Sime PJ: High-dose but not low-dose mainstream cigarette smoke suppresses allergic airway inflammation by inhibiting T cell function. Am J Physiol Lung Cell Mol Physiol. 2008, 295 (3): L412-421. 10.1152/ajplung.00392.2007.PubMed CentralPubMedGoogle Scholar
  120. Chang JC, Distler SG, Kaplan AM: Tobacco smoke suppresses T cells but not antigen-presenting cells in the lung-associated lymph nodes. Toxicol Appl Pharmacol. 1990, 102 (3): 514-523. 10.1016/0041-008X(90)90046-W.PubMedGoogle Scholar
  121. Johnson JD, Houchens DP, Kluwe WM, Craig DK, Fisher GL: Effects of mainstream and environmental tobacco smoke on the immune system in animals and humans: a review. Crit Rev Toxicol. 1990, 20 (5): 369-395. 10.3109/10408449009089870.PubMedGoogle Scholar
  122. Sopori ML, Cherian S, Chilukuri R, Shopp GM: Cigarette smoke causes inhibition of the immune response to intratracheally administered antigens. Toxicol Appl Pharmacol. 1989, 97 (3): 489-499. 10.1016/0041-008X(89)90254-8.PubMedGoogle Scholar
  123. Kinane DF, Chestnutt IG: Smoking and periodontal disease. Crit Rev Oral Biol Med. 2000, 11 (3): 356-365.PubMedGoogle Scholar
  124. Barbour SE, Nakashima K, Zhang JB, Tangada S, Hahn CL, Schenkein HA, Tew JG: Tobacco and smoking: environmental factors that modify the host response (immune system) and have an impact on periodontal health. Crit Rev Oral Biol Med. 1997, 8 (4): 437-460.PubMedGoogle Scholar
  125. Pitzer JE, Del Zoppo GJ, Schmid-Schonbein GW: Neutrophil activation in smokers. Biorheology. 1996, 33 (1): 45-58. 10.1016/0006-355X(96)00004-2.PubMedGoogle Scholar
  126. Prescott SL: Effects of early cigarette smoke exposure on early immune development and respiratory disease. Paediatr Respir Rev. 2008, 9 (1): 3-9. 10.1016/j.prrv.2007.11.004.PubMedGoogle Scholar
  127. de Jonge WJ, Ulloa L: The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol. 2007Google Scholar
  128. Scott DAPR: The influence of tobacco smoking on adhesion molecule profiles. Tobacco Induced Diseases. 2002, 1 (1): 7-25.PubMed CentralPubMedGoogle Scholar
  129. Sopori M: Effects of cigarette smoke on the immune system. Nat Rev Immunol. 2002, 2 (5): 372-377. 10.1038/nri803.PubMedGoogle Scholar
  130. Bridger S, Lee JC, Bjarnason I, Jones JE, Macpherson AJ: In siblings with similar genetic susceptibility for inflammatory bowel disease, smokers tend to develop Crohn's disease and non-smokers develop ulcerative colitis. Gut. 2002, 51 (1): 21-25. 10.1136/gut.51.1.21.PubMed CentralPubMedGoogle Scholar
  131. Bundred NJ, Dover MS, Aluwihare N, Faragher EB, Morrison JM: Smoking and periductal mastitis. BMJ. 1993, 307 (6907): 772-773.PubMed CentralPubMedGoogle Scholar
  132. Grossi SG, Genco RJ, Machtei EE, Ho AW, Koch G, Dunford R, Zambon JJ, Hausmann E: Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol. 1995, 66 (1): 23-29.PubMedGoogle Scholar
  133. Hammaren-Malmi S, Saxen H, Tarkkanen J, Mattila PS: Passive smoking after tympanostomy and risk of recurrent acute otitis media. Int J Pediatr Otorhinolaryngol. 2007, 71 (8): 1305-1310. 10.1016/j.ijporl.2007.05.010.PubMedGoogle Scholar
  134. Kovesi T, Corey M, Levison H: Passive smoking and lung function in cystic fibrosis. Am Rev Respir Dis. 1993, 148 (5): 1266-1271.PubMedGoogle Scholar
  135. Mahid SS, Minor KS, Stromberg AJ, Galandiuk S: Active and passive smoking in childhood is related to the development of inflammatory bowel disease. Inflamm Bowel Dis. 2007, 13 (4): 431-438. 10.1002/ibd.20070.PubMedGoogle Scholar
  136. Neumayer L, Hosokawa P, Itani K, El-Tamer M, Henderson WG, Khuri SF: Multivariable predictors of postoperative surgical site infection after general and vascular surgery: results from the patient safety in surgery study. J Am Coll Surg. 2007, 204 (6): 1178-1187. 10.1016/j.jamcollsurg.2007.03.022.PubMedGoogle Scholar
  137. Pastor P, Medley F, Murphy TV: Invasive pneumococcal disease in Dallas County, Texas: results from population-based surveillance in 1995. Clin Infect Dis. 1998, 26 (3): 590-595. 10.1086/514589.PubMedGoogle Scholar
  138. Smyth A, O'Hea U, Williams G, Smyth R, Heaf D: Passive smoking and impaired lung function in cystic fibrosis. Arch Dis Child. 1994, 71 (4): 353-354. 10.1136/adc.71.4.353.PubMed CentralPubMedGoogle Scholar
  139. Stuart JM, Cartwright KA, Robinson PM, Noah ND: Effect of smoking on meningococcal carriage. Lancet. 1989, 2 (8665): 723-725. 10.1016/S0140-6736(89)90781-2.PubMedGoogle Scholar
  140. Furlong AJ, al-Nakib L, Knox WF, Parry A, Bundred NJ: Periductal inflammation and cigarette smoke. J Am Coll Surg. 1994, 179 (4): 417-420.PubMedGoogle Scholar
  141. Dixon JM, Ravisekar O, Chetty U, Anderson TJ: Periductal mastitis and duct ectasia: different conditions with different aetiologies. Br J Surg. 1996, 83 (6): 820-822. 10.1002/bjs.1800830630.PubMedGoogle Scholar
  142. Ah MK, Johnson GK, Kaldahl WB, Patil KD, Kalkwarf KL: The effect of smoking on the response to periodontal therapy. J Clin Periodontol. 1994, 21 (2): 91-97. 10.1111/j.1600-051X.1994.tb00285.x.PubMedGoogle Scholar
  143. Apatzidou DA, Riggio MP, Kinane DF: Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol. 2005, 32 (9): 973-983. 10.1111/j.1600-051X.2005.00788.x.PubMedGoogle Scholar
  144. Bergstrom J: Tobacco smoking and chronic destructive periodontal disease. Odontology. 2004, 92 (1): 1-8. 10.1007/s10266-004-0043-4.PubMedGoogle Scholar
  145. Bergstrom J: Influence of tobacco smoking on periodontal bone height. Long-term observations and a hypothesis. J Clin Periodontol. 2004, 31 (4): 260-266. 10.1111/j.1600-051X.2004.00475.x.PubMedGoogle Scholar
  146. Bergstrom J: Periodontitis and smoking: an evidence-based appraisal. J Evid Based Dent Pract. 2006, 6 (1): 33-41. 10.1016/j.jebdp.2005.12.018.PubMedGoogle Scholar
  147. Bergstrom J, Eliasson S, Dock J: A 10-year prospective study of tobacco smoking and periodontal health. J Periodontol. 2000, 71 (8): 1338-1347. 10.1902/jop.2000.71.8.1338.PubMedGoogle Scholar
  148. Gonzalez YM, De Nardin A, Grossi SG, Machtei EE, Genco RJ, De Nardin E: Serum cotinine levels, smoking, and periodontal attachment loss. J Dent Res. 1996, 75 (2): 796-802.PubMedGoogle Scholar
  149. Haffajee AD, Socransky SS: Relationship of cigarette smoking to attachment level profiles. J Clin Periodontol. 2001, 28 (4): 283-295. 10.1034/j.1600-051x.2001.028004283.x.PubMedGoogle Scholar
  150. MacFarlane GD, Herzberg MC, Wolff LF, Hardie NA: Refractory periodontitis associated with abnormal polymorphonuclear leukocyte phagocytosis and cigarette smoking. J Periodontol. 1992, 63 (11): 908-913.PubMedGoogle Scholar
  151. Tomar SL, Asma S: Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol. 2000, 71 (5): 743-751. 10.1902/jop.2000.71.5.743.PubMedGoogle Scholar
  152. Tuvlin JA, Raza SS, Bracamonte S, Julian C, Hanauer SB, Nicolae DL, King AC, Cho JH: Smoking and inflammatory bowel disease: trends in familial and sporadic cohorts. Inflamm Bowel Dis. 2007, 13 (5): 573-579. 10.1002/ibd.20043.PubMedGoogle Scholar
  153. Mokbel M, Carbonnel F, Beaugerie L, Gendre JP, Cosnes J: [Effect of smoking on the long-term course of ulcerative colitis]. Gastroenterol Clin Biol. 1998, 22 (11): 858-862.PubMedGoogle Scholar
  154. Johnson GJ, Cosnes J, Mansfield JC: Review article: smoking cessation as primary therapy to modify the course of Crohn's disease. Aliment Pharmacol Ther. 2005, 21 (8): 921-931. 10.1111/j.1365-2036.2005.02424.x.PubMedGoogle Scholar
  155. Kane SV, Flicker M, Katz-Nelson F: Tobacco use is associated with accelerated clinical recurrence of Crohn's disease after surgically induced remission. J Clin Gastroenterol. 2005, 39 (1): 32-35.PubMedGoogle Scholar
  156. Ilicali OC, Keles N, De er K, Sa un OF, Guldiken Y: Evaluation of the effect of passive smoking on otitis media in children by an objective method: urinary cotinine analysis. Laryngoscope. 2001, 111 (1): 163-167. 10.1097/00005537-200101000-00028.PubMedGoogle Scholar

Copyright

© Bagaitkar et al; licensee BioMed Central Ltd. 2008

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.