NIH Public Access
Author Manuscript
Oral Dis. Author manuscript; available in PMC 2008 February 28.
Oral Dis. 2007 November ; 13(6): 508–512.
Oral biofilms, periodontitis, and pulmonary infections
S Paju1,2 and FA Scannapieco3
1Institute of Dentistry, University of Helsinki, Helsinki, Finland 2Department of Oral and MaxillofacialDiseases, Helsinki University Central Hospital, Helsinki, Finland 3Department of Oral Biology, School ofDental Medicine, University at Buffalo, State University of New York, Buffalo, NY, USA Abstract
Bacteria from the oral biofilms may be aspirated into the respiratory tract to influence the initiationand progression of systemic infectious conditions such as pneumonia. Oral bacteria, poor oralhygiene, and periodontitis seem to influence the incidence of pulmonary infections, especiallynosocomial pneumonia episodes in high-risk subjects. Improved oral hygiene has been shown to reduce the occurrence of nosocomial pneumonia, both in mechanically-ventilated hospital patientsand non-ventilated nursing home residents. It appears that oral colonization by potential respiratorypathogens, possibly fostered by periodontitis, and possibly by bacteria specific to the oral cavity orto periodontal diseases contribute to pulmonary infections. Thus, oral hygiene will assume an evenmore important role in the care of high-risk subjects – patients in the hospital intensive care and theelderly. The present paper critically reviews the recent literature on the effect of oral biofilms andperiodontitis on pneumonia.
infectious diseases; oral hygiene; pathogenesis; periodontitis; pneumonia Pneumonia is an infection of the lungs caused by bacteria, mycoplasma, viruses, fungi, orparasites. Bacterial pneumonia is a common and significant cause of mortality and morbidityin human populations. Pneumonia together with influenza is a top ten cause of death in theworld, and in elderly nursing home residents the leading cause of death. Pneumonia also resultsin morbidity and considerable decline in the individual quality of life as well as in increased medical care costs for the healthcare system. Bacterial pneumonia includes community-acquired pneumonia and hospital-acquired (nosocomial) pneumonia. Nosocomial pneumonia,occurring >48–72 h after admission to a hospital or nursing home, can be divided into twosubtypes: ventilator-associated pneumonia (VAP) and non-VAP. Pneumonia accounts for 10%of infections in intensive care units (ICU) being the most common infection in this hospitalsetting (Vincent et al, 1995). The onset of pneumonia can easily double the length of thepatient’s hospital stay, and the cost of VAP treatment has been estimated to average as high as$40 000 per patient (Rello et al, 2002). Pneumonia is also prevalent in nursing homes,comprising 13–48% of all infections (Crossley and Thurn, 1989). The mortality rate ofnosocomial pneumonia can be as high as 25%.
The oral cavity may be an important source of bacteria that cause infections of the lungs. Dentalplaque, a tooth-borne biofilm that initiates periodontal disease and dental caries may alsoinfluence the initiation and progression of pneumonia because of relocalization of the bacteria Correspondence: Susanna Paju, Institute of Dentistry, PO Box 63, University of Helsinki, 00014 Helsinki, Finland. Tel / fax: +358919125194, E-mail: [email protected].
from the biofilm into the respiratory tract. Bacteria causing community-acquired pneumoniaare typically species that normally colonize the oropharynx such as Streptococcus pneumoniae, Haemophilus influenzae, and Mycoplasma pneumoniae. Nosocomial pneumoniais, in contrast, often caused by bacteria that are not common members of the oropharyngealflora such as Pseudomonas aeruginosa, Staphylococcus aureus, and enteric Gram-negativebacteria. These organisms populate the oral cavity in certain settings, for example ininstitutionalized subjects and in people living in areas served by unsanitary water supplies(Scannapieco, 1999). Respiratory pathogens, such as S. aureus, P. aeruginosa, and Escherichiacoli, have been found to be present in substantial numbers on the teeth in both institutionalizedelders (Russell et al, 1999) and intensive care patients (Scannapieco et al, 1992). In this reviewwe concentrate on the possible effect of oral biofilms and periodontitis on pneumonia.
Mechanisms behind the association between oral bacteria/periodontitis and
One cubic millimeter of dental plaque contains about 100 million bacteria (Thoden van Velzenet al, 1984) and may serve as a persistent reservoir for potential pathogens, both oral andrespiratory bacteria. It is likely that oral and respiratory bacteria in the dental plaque are shedinto the saliva and are then aspirated into the lower respiratory tract and the lungs to causeinfection (Scannapieco, 1999; Scannapieco et al, 2001). Cytokines and enzymes induced from the periodontally inflamed tissues by the oral biofilm may also be transferred into the lungswhere they may stimulate local inflammatory processes preceding colonization of pathogensand the actual lung infection (Scannapieco, 1999; Scannapieco et al, 2001). Other possiblemechanisms of pulmonary infection are inhalation of airborne pathogens or translocation ofbacteria from local infections via bacteremia.
In a healthy subject, the respiratory tract is able to defend against aspirated bacteria. Patientswith diminished salivary flow, decreased cough reflex, swallowing disorders, poor ability toperform good oral hygiene, or other physical disabilities have a high risk for pulmonaryinfections. Mechanically ventilated patients in ICUs with no ability to clear oral secretions byswallowing or by coughing, are at risk for VAP especially if the ventilation lasts for more than48 h (Estes and Meduri, 1995). Oral bacterial load increases during intubation and higher dentalplaque scores predict risk of pneumonia (Munro et al, 2006). Anaerobic bacteria are frequentlyfound to colonize the lower respiratory tract in mechanically-ventilated patients (Estes andMeduri, 1995; Robert et al, 2003). Colonization of bacteria in the digestive tract has beensuggested to be a source for nosocomial pneumonia, but recently oral and dental bacterialcolonization has been proposed to be the major source of bacteria implicated in the etiologyof VAP (Garcia, 2005).
In the institutionalized elderly the aspiration of saliva seems to be the main route of bacteriainto the lungs causing aspiration pneumonia. Dysphagia seems to be an important risk factor,even a predictor, for aspiration pneumonia (Langmore et al, 1998). The major oral and dentalrisk factors for aspiration pneumonia in veteran residents of nursing homes were number ofdecayed teeth, periodontitis, oral S. aureus colonization, and requirement of help feeding(Terpenning et al, 2001). Inadequate oral care and swallowing diffculties were associated withpneumonia in 613 elderly nursing home patients (Quagliarello et al, 2005).
Studies on the relationship between the oral microflora /periodontitis and
Very little data on the relationship of oral microflora to community-acquired pneumonia areavailable. Most of the studies have been conducted in populations with a high prevalence ofpneumonia, such as hospitalized patients and the elderly in nursing homes. An epidemiologic Oral Dis. Author manuscript; available in PMC 2008 February 28.
study found no association between periodontal state or poor oral hygiene and acute respiratorydisease in the community-dwelling population (Scannapieco et al, 1998), but ample evidence exists to support a role for oral bacteria and/or poor oral health in the pathogenesis ofnosocomial pneumonia. Poor oral health, dental plaque, or oropharyngeal bacterialcolonization have been associated with the occurrence of pneumonia in hospitalized or ICUpatients (Scannapieco et al, 1992; Bonten et al, 1996; Garrouste-Orgeas et al, 1997; Fourrieret al, 1998; Preston et al, 1999; El-Solh et al, 2004), but a clear relationship betweenperiodontitis and pneumonia has not always been found (Chabrand et al, 1986; Treloar andStechmiller, 1995). Higher plaque scores, bacterial presence in saliva, or colonization in theoropharynx seem to be associated with pneumonia in elderly nursing home patients (Mojonet al, 1997; Langmore et al, 1998; Russell et al, 1999; Terpenning et al, 2001).
Recent systematic reviews of the literature substantiate the link between poor oral health andpneumonia (Scannapieco et al, 2003; Azarpazhooh and Leake, 2006), but more studies on thepossible role of periodontitis are needed. Dentate status may be a risk for pneumonia andrespiratory tract infections – patients with natural teeth developed aspiration pneumonia moreoften than edentulous subjects (Terpenning et al, 1993; Mojon et al, 1997). Cariogenic bacteriaand periodontal pathogens in saliva or dental plaque are found to be risk factors for aspirationpneumonia in nursing home patients (Langmore et al, 1998; Terpenning et al, 2001). It is wellknown that the teeth and gingival margin are places that favour bacterial colonization, and periodontal pockets may serve as reservoirs for potential pathogens for pneumonia. Previousstudies have shown that enteric bacteria colonize periodontal pockets (Slots et al, 1988; Ramset al, 1990). Periodontitis together with poor oral hygiene or by facilitating colonization ofdental plaque may promote pneumonia.
Intervention studies on the role of improved oral cleaning in reducing
Oral interventions to reduce pulmonary infections have been examined in both mechanicallyventilated ICU patients and non-ventilated elderly patients. These studies included chemicalintervention using topical antimicrobial agents and traditional oral mechanical hygieneperformed by a professional.
Hospitalized ICU patients seem to benefit from daily oral cleansing. Studies have shown thatthe use of oral topical chlorhexidine (CHX) reduces pneumonia in mechanically ventilatedpatients and may even decrease the need of systemic IV antibiotics or shorten the duration ofmechanical ventilation in the ICU (DeRiso et al, 1996; Fourrier et al, 2000; Genuit et al,2001; Koeman et al, 2006). Moreover, oral application of CHX in the early post-intubation period lowers the numbers of cultivable oral bacteria and may delay the development of VAP(Grap et al, 2004). Studies validating the effectiveness of oral CHX on reducing pneumoniaare not unanimous. For example, Fourrier et al found that gingival decontamination with CHXgel significantly decreased the oropharyngeal colonization by bacteria in ventilated patients,but was not sufficient to reduce the incidence of respiratory infections (Fourrier et al, 2005).
Another study by Houston et al (2002) reported that a significant reduction in pneumonia usingCHX rinse in ICU patients was achieved only after 24 h of intubation. However, the efficacyof oral CHX decontamination to reduce VAP needs further investigation as no clear reductionin mortality rate has been shown. In addition to CHX, other anti-plaque agents have beeninvestigated. The use of antimicrobial gels including polymyxin B sulfate, neomycin sulfate,and vancomycin hydrochloride (Pugin et al, 1991) or gentamicin/colistin/vancomycin(Bergmans et al, 2001) have also been shown to reduce VAP. Recently, the first study showingthat mechanical oral care in combination with povidone iodine significantly decreasespneumonia in ventilated ICU patients was published (Mori et al, 2006). This suggests that tooth Oral Dis. Author manuscript; available in PMC 2008 February 28.
brushing combined with a topical antimicrobial agent is a promising method for oral cleansingof mechanically ventilated patients.
Institutionalized but non-ventilated patients, mainly elders living in nursing homes, appear tobenefit from improved oral care by showing lower levels of oral bacteria and fewer pneumoniaepisodes and febrile days. Daily tooth brushing and topical oral swabbing with povidone iodinesignificantly decreased pneumonia in residents in long-term care facilities (Yoneyama et al,1999, 2002; Yoshida et al, 2001). However, in an earlier study by the same research group,oral care with both brushing and antimicrobial gargling had an effect only on febrile days butnot on the incidence of pneumonia (Yoneyama et al, 1996). Interestingly, professional cleaningby a dental hygienist once a week significantly reduced the prevalence of fever and fatalpneumonia in 141 elderly patients in nursing homes (Adachi et al, 2002). Similar once-a-weekprofessional oral cleaning significantly reduced influenza infections in an elderly population(Abe et al, 2006). Dental plaque is known to form clearly visible masses in the teeth in a fewdays, but these studies suggest that improved oral care even without chemical agents and evenif not performed daily not only reduces the oral bacterial, viral, and fungal load, but may havean effect on reducing the risk of pneumonia. Therefore, more studies are needed to find theeasiest oral decontamination methods to reduce pulmonary infections in elderly nursing homepatients.
Our previously published systematic literature review revealed that interventions improving oral hygiene by mechanical and/or topical chemical disinfection or antibiotics reduce theincidence of hospital-acquired pneumonia by an average of 40% (Scannapieco et al, 2003).
Oral cleansing reduces pneumonia in both edentulous and dentate subjects, suggesting that oralcolonization of bacteria contributes to nosocomial pneumonia to a greater extent thanperiodontitis. However, intervention studies on the treatment of periodontitis on the incidenceof pneumonia have not been performed due to the complexities required in investigating ICUor bed-bound nursing home patients. In edentulous people, dentures may easily serve as asimilar reservoir as teeth for oral and respiratory bacteria if not cleaned properly and daily.
Conclusions and future visions
Poor oral health, dependence on help conducting daily oral hygiene, oral colonization ofperiodontal and respiratory pathogens, all possibly influenced by periodontitis, are associatedwith nosocomial pneumonia. A direct causal relationship between periodontitis and pneumoniahas not been established, however. Based on the studies reviewed here it seems that oralcolonization by potential respiratory pathogens contributes to pulmonary infections. Thespecific contribution of periodontitis per se to pneumonia risk is presently unknown. It will be difficult to determine whether periodontitis is related to pneumonia in ICU subjects, forexample, due to the limited access to these patients’ oral cavity, and the rapid turnover ofpatients in the hospital that presents logistical challenges to such research. Thus, oral hygieneof both dentate and edentulous subjects will assume an even more important role in elder care.
Chronic periodontal infections are common – the prevalence of severe periodontitis in Westerncountries has been estimated to be 5–15%. Pneumonia and other respiratory infections arecommon in community-dwelling populations but especially in high-risk subjects such asmechanically-ventilated ICU patients and residents in long-term care facilities. With improvedoral hygiene and preventative approaches to dental care, people are able to keep their naturalteeth longer, even for life. Edentulousness will someday be a rare phenomenon; in the futurethere will be more elderly dentate people, having more teeth than ever, but who will also haveimpaired ability to perform oral hygiene, and hence more cases of periodontal diseases. Toassure that improved knowledge and methods to save people’s natural teeth are not taking us Oral Dis. Author manuscript; available in PMC 2008 February 28.
from one problem to another, emphasis on the importance of good oral hygiene and periodontaltreatment, especially in subjects who are in high risk for pulmonary infections, is crucial.
The authors are supported by grants 209152 and 211117 (SP) from the Academy of Finland and DE014685 (FAS)from the National Institutes of Health (USA).
Abe S, Ishihara K, Adachi M, et al. Professional oral care reduces influenza infection in elderly. Arch Gerontol Geriatr 2006;43:157–164. [PubMed: 16325937] Adachi M, Ishihara K, Abe S, Okuda K, Ishikawa T. Effect of professional oral health care on the elderly living in nursing homes. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;94:191–195.
[PubMed: 12221387] Azarpazhooh A, Leake JL. Systematic review of the association between respiratory diseases and oral health. J Periodontol 2006;77:1465–1482. [PubMed: 16945022] Bergmans DC, Bonten MJ, Gaillard CA, et al. Prevention of ventilator-associated pneumonia by oral decontamination: a prospective, randomized, double-blind, placebo-controlled study. Am J Respir CritCare Med 2001;164:382–388. [PubMed: 11500337] Bonten MJ, Bergmans DC, Ambergen AW, et al. Risk factors for pneumonia, and colonization of respiratory tract and stomach in mechanically ventilated ICU patients. Am J Respir Crit Care Med Chabrand F, Allamand JM, Duroux P, et al. Are orodental infectious foci responsible for bacterial pneumopathies? A statistical study. Rev Stomatol Chir Maxillofac 1986;87:73–77. [PubMed:3460159] Crossley KB, Thurn JR. Nursing home-acquired pneumonia. Semin Respir Infect 1989;4:64–72.
DeRiso AJ 2nd, Ladowski JS, Dillon TA, Justice JW, Peterson AC. Chlorhexidine gluconate 0.12% oral rinse reduces the incidence of total nosocomial respiratory infection and nonprophylactic systemicantibiotic use in patients undergoing heart surgery. Chest 1996;109:1556–1561. [PubMed: 8769511] El-Solh AA, Pietrantoni C, Bhat A, et al. Colonization of dental plaques: a reservoir of respiratory pathogens for hospital-acquired pneumonia in institutionalized elders. Chest 2004;126:1575–1582.
[PubMed: 15539730] Estes RJ, Meduri GU. The pathogenesis of ventilator-associated pneumonia: I. Mechanisms of bacterial transcolonization and airway inoculation. Intensive Care Med 1995;21:365–383. [PubMed:7650262] Fourrier F, Duvivier B, Boutigny H, Roussel-Delvallez M, Chopin C. Colonization of dental plaque: a source of nosocomial infections in intensive care unit patients. Crit Care Med 1998;26:301–308.
[PubMed: 9468169] Fourrier F, Cau-Pottier E, Boutigny H, et al. Effects of dental plaque antiseptic decontamination on bacterial colonization and nosocomial infections in critically ill patients. Intensive Care Med2000;26:1239–1247. [PubMed: 11089748] Fourrier F, Dubois D, Pronnier P, et al. Effect of gingival and dental plaque antiseptic decontamination on nosocomial infections acquired in the intensive care unit: a double-blind placebo-controlledmulticenter study. Crit Care Med 2005;33:1728–1735. [PubMed: 16096449] Garcia R. A review of the possible role of oral and dental colonization on the occurrence of health care- associated pneumonia: underappreciated risk and a call for interventions. Am J Infect Control2005;33:527–541. [PubMed: 16260328] Garrouste-Orgeas M, Chevret S, Arlet G, et al. Oropharyngeal or gastric colonization and nosocomial pneumonia in adult intensive care unit patients. A prospective study based on genomic DNA analysis.
Am J Respir Crit Care Med 1997;156:1647–1655. [PubMed: 9372689] Genuit T, Bochicchio G, Napolitano LM, McCarter RJ, Roghman MC. Prophylactic chlorhexidine oral rinse decreases ventilator-associated pneumonia in surgical ICU patients. Surg Infect (Larchmt)2001;2:5–18. [PubMed: 12594876] Oral Dis. Author manuscript; available in PMC 2008 February 28.
Grap MJ, Munro CL, Elswick RK Jr, Sessler CN, Ward KR. Duration of action of a single, early oral application of chlorhexidine on oral microbial flora in mechanically ventilated patients: a pilot study.
Heart Lung 2004;33:83–91. [PubMed: 15024373] Houston S, Hougland P, Anderson JJ, et al. Effectiveness of 0.12% chlorhexidine gluconate oral rinse in reducing prevalence of nosocomial pneumonia in patients undergoing heart surgery. Am J Crit Care2002;11:567–570. [PubMed: 12425407] Koeman M, van der Ven AJ, Hak E, et al. Oral decontamination with chlorhexidine reduces the incidence of ventilator-associated pneumonia. Am J Respir Crit Care Med 2006;173:1348–1355. [PubMed:16603609] Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia 1998;13:69–81. [PubMed: 9513300] Mojon P, Budtz-Jorgensen E, Michel JP, Limeback H. Oral health and history of respiratory tract infection in frail institutionalised elders. Gerodontology 1997;14:9–16. [PubMed: 9610298] Mori H, Hirasawa H, Oda S, et al. Oral care reduces incidence of ventilator-associated pneumonia in ICU populations. Intensive Care Med 2006;32:230–236. [PubMed: 16435104] Munro CL, Grap MJ, Elswick RK Jr, et al. Oral health status and development of ventilator-associated pneumonia: a descriptive study. Am J Crit Care 2006;15:453–460. [PubMed: 16926366] Preston AJ, Gosney MA, Noon S, Martin MV. Oral flora of elderly patients following acute medical admission. Gerontology 1999;45:49–52. [PubMed: 9852381] Pugin J, Auckenthaler R, Lew DP, Suter PM. Oropharyngeal decontamination decreases incidence of ventilator-associated pneumonia. A randomized, placebo-controlled, double-blind clinical trial.
JAMA 1991;265:2704–2710. [PubMed: 2023353] Quagliarello V, Ginter S, Han L, et al. Modifiable risk factors for nursing home-acquired pneumonia.
Clin Infect Dis 2005;40:1–6. [PubMed: 15614684] Rams TE, Babalola OO, Slots J. Subgingival occurrence of enteric rods, yeasts and staphylococci after systemic doxycycline therapy. Oral Microbiol Immunol 1990;5:166–168. [PubMed: 2080072] Rello J, Ollendorf DA, Oster G, et al. Epidemiology and outcomes of ventilator-associated pneumonia in a large US database. Chest 2002;122:2115–2121. [PubMed: 12475855] Robert R, Grollier G, Frat JP, et al. Colonization of lower respiratory tract with anaerobic bacteria in mechanically ventilated patients. Intensive Care Med 2003;29:1062–1068. [PubMed: 12698243] Russell SL, Boylan RJ, Kaslick RS, Scannapieco FA, Katz RV. Respiratory pathogen colonization of the dental plaque of institutionalized elders. Spec Care Dentist 1999;19:128–134. [PubMed: 10860077] Scannapieco FA. Role of oral bacteria in respiratory infection. J Periodontol 1999;70:793–802. [PubMed: Scannapieco FA, Stewart EM, Mylotte JM. Colonization of dental plaque by respiratory pathogens in medical intensive care patients. Crit Care Med 1992;20:740–745. [PubMed: 1597025] Scannapieco FA, Papandonatos GD, Dunford RG. Associations between oral conditions and respiratory disease in a national sample survey population. Ann Periodontol 1998;3:251–256. [PubMed:9722708] Scannapieco FA, Wang B, Shiau HJ. Oral bacteria and respiratory infection: effects on respiratory pathogen adhesion and epithelial cell proinflammatory cytokine production. Ann Periodontol2001;6:78–86. [PubMed: 11887474] Scannapieco FA, Bush RB, Paju S. Associations between periodontal disease and risk for nosocomial bacterial pneumonia and chronic obstructive pulmonary disease. A systematic review. AnnPeriodontol 2003;8:54–69. [PubMed: 14971248] Slots J, Rams TE, Listgarten MA. Yeasts, enteric rods and pseudomonads in the subgingival flora of severe adult periodontitis. Oral Microbiol Immunol 1988;3:47–52. [PubMed: 3268751] Terpenning M, Bretz W, Lopatin D, et al. Bacterial colonization of saliva and plaque in the elderly. Clin Infect Dis 1993;16(Suppl 4):S314–S316. [PubMed: 8324138] Terpenning MS, Taylor GW, Lopatin DE, et al. Aspiration pneumonia: dental and oral risk factors in an older veteran population. J Am Geriatr Soc 2001;49:557–563. [PubMed: 11380747] Thoden van Velzen SK, Abraham-Inpijn L, Moorer WR. Plaque and systemic disease: a reappraisal of the focal infection concept. J Clin Periodontol 1984;11:209–220. [PubMed: 6368612] Oral Dis. Author manuscript; available in PMC 2008 February 28.
Treloar DM, Stechmiller JK. Use of a clinical assessment tool for orally intubated patients. Am J Crit Vincent JL, Bihari DJ, Suter PM, et al. The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) Study. EPICInternational Advisory Committee. JAMA 1995;274:639–644. [PubMed: 7637145] Yoneyama T, Hashimoto K, Fukuda H, et al. Oral hygiene reduces respiratory infections in elderly bed- bound nursing home patients. Arch Gerontol Geriatr 1996;22:11–19. [PubMed: 15374188] Yoneyama T, Yoshida M, Matsui T, Sasaki H. Oral care and pneumonia. Oral Care Working Group.
Yoneyama T, Yoshida M, Ohrui T, et al. Oral care reduces pneumonia in older patients in nursing homes.
J Am Geriatr Soc 2002;50:430–433. [PubMed: 11943036] Yoshida M, Yoneyama T, Akagawa Y. Oral care reduces pneumonia of elderly patients in nursing homes, irrespective of dentate or edentate status. Nippon Ronen Igakkai Zasshi 2001;38:481–483. [PubMed:11523155] Oral Dis. Author manuscript; available in PMC 2008 February 28.

Source: http://www.cemoi.com.br/artigos_cientificos/OI_21.pdf

At 24 i realized i had a problem with food

At 24 I realized I had a problem with food. I have struggled with an eating disorder, since I was fourteen. I of course felt all my habits with food were normal. To my unhealthy surprise at 24 I came to terms, with binging/compulsive eating ECT. During this time I had become very dependent on anti- depressants. I have always struggled with acne. After several try’s of medications my doctor reco


DE VEZ EN CUANDO Adrede, contra el silencio aleve que no tienen alas los verdaderos ángeles. Carlos Pellicer Por René Rodríguez Soriano | © MEDIAISLA Nada puedo hablar sobre la nada sin rondar la otra orilla. Ya ha dicho el Gabo que su abuelo dijo que no existe, y contundente y sin mitrado confirmó José que virgen y desnuda es un proyecto de ser, lejos de la esencia

© 2010-2017 Pdf Pills Composition