A. Cagna
Private Practitioner, Turin

G. L. Princi
Private Practitioner, Messina

Cigarette Smoke As a Risk Factor of Periodontal Disease. A Rewiew.

Abstract
A thorough review of the literature on the negative effects caused by cigarette smoke on periodontal tissues and surgical treatments is presented.

The various anatomical and clinical parameters that may be of interest for the study of periodontal disease in smokers have been evaluated. Recents publications related to the etiology and pathogenesis of periodontal disease in smokers have been critically reviewed.

Among the arguments considered, special attention has been devoted to the analysis of the surgery period, in particular new techniques of guided tissue regeneration and the covering of exposed root surfaces.

Introduction
Cigarette smoke represents one of the major risk factors for numerous pathologies, not only of neoplastic type. It has been estimated that in Europe alone it causes around 400,000 deaths/year due to malignancies affecting lung, upper respiratory and digestive tracts, bladder and kidney. Moreover, tobacco is responsible for 25 % of deaths due to cardiovascular diseases and for 80 % of chronic respiratory illnesses.

In the dental field, numerous clinical studies have demonstrated a correlation between cigarette smoke, periodontal diseases and tumors of the oral cavity.

A few studies have underlined that smokers are less prone to maintain a good oral hygiene, compared to non-smokers. However, recent studies showed a significant alteration of the normal periodontal anatomy, that may be directly linked to smoke rather than to the reduced capacity of smokers to maintain an adequate plaque control.

Clinical features
Physical examination of smoking patients presenting with a periodontal disease shows a fibrotic gingival margin with thickened margins; redness and edema are not always evident, even in more advanced stages of the disease.

Examination with a probe shows a higher probing index, especially in the vestibular sectors of anterior teeth and in the palatal zones of posterior teeth. Gingival recessions localized in the anterior vestibular zone are more frequently noted in smokers. Moreover, a higher incidence of periodontal disease is found in young smokers compared to non-smokers peers.

Smoke has been shown to reduce the presentation of clinical signs of inflammation (bleeding, edema, etc.), although it may be associated with a remarkable amount of plaque and calculus (tartar), and with a higher incidence of pathologic changes, such as loss of attachment, loss of bone support and pocketing.

These data show that smoking patients will develop the symptoms of periodontal disease at a later time, when the pathology is in an advanced stage, so that the clinician will likely underestimate the disease.

On the other hand, smoke cessation will favour an increase in bleeding following routine oral hygiene manoeuvres and, more generally, a recurrence of typical symptoms of gingivitis. This phase may last a few months up to one year; afterwards the gum is likely to resume normal anatomic features while losing the thickened fibrotic aspect. Moreover, loss of attachment will stop or be significantly reduced in most cases.

Therefore, it is important that patients be informed of a possible acute phase of the disease a few week after smoke cessation, in order to become motivated and get informed about the initial difficulties.

Epidemiology
In the past, a few scientific contributions have underlined that the highest rate of smokers is found among lower social classes in terms of economic and cultural levels; this fact might explain why these patients have the lowest oral hygiene level.

Linden et al. have evaluated pouch depth, loss of attachment, plaque indexes, presence of calculus and bleeding index in a group of 82 patients (21 smokers, 61 non-smokers) aged 20-33 years, who had been followed as dental outpatients for one year. Smoking patients had a higher number of sites with a probing depth > 4 mm and a loss of attachment > 2 mm. The study showed that even among patients who regularly attended dental surgery and were therefore motivated at maintaining a good oral hygiene, smoke was the greatest risk factor and was associated with the fastest periodontal destruction.

Bergstrom et al., on the other hand, have evaluated the smoke-associated bone resorption in a group of 210 Swedish hygienists aged 24-60 years. Of these, 30 % were smokers, 2 % were ex-smokers while 38 % never smoked. Intra-oral bite-wing Rx were used to evaluate bone loss. The enamel-cement junction and the apex of the interdental-sectum on the mesial and distal aspects of five posterior teeth, with the exception of the mesial surfaces of first premolars and of the distal surfaces of second premolars, were assumed as reference points. A high oral hygiene level was found both in smokers and non-smokers, however smokers had a higher distance between the interdental bone sept and the enamel-cement junction; this distance was significantly higher among smokers with a daily consumption > 10 cigarettes. Therefore, this study shows that the interproximal bone resorption was significantly higher in smokers than in non-smokers.

Locker e Leake analyzed the occurrence of bone loss in a group of 624 randomly chosen individuals from 4 communities of Ontario, Canada. Mean age was 62.3 years (55.4 % women, 95.5 % whites). The level of connective attachment was measured over all teeth, in two sites/tooth. For each subject, the percentage of sites with a loss of attachment > 2 mm and the percentage of subjects with a mean loss of attachment considered as severe (> 3.83 mm) were then calculated. Compared to non-smokers, regular smokers showed a higher percentage of sites with loss of attachment > 2 mm (85 % vs 16 %) and a greater number of subjects with severe loss of attachment (34 % vs 16 %).

Bergstrom et al. and MacFarlane et al. found a high incidence of smokers among patients affected by rapidly progressing periodontitis and acute necrotizing ulcerative gingivitis; in patients affected by refractory periodontitis, smokers amounted to 90 %.

When compared to former smokers, smokers showed greater periodontal damage with higher indexes of probing depth, loss of attachment and bone resorption.

Etiology
The presence of common bacteria responsible for periodontal destruction and the possible differences in the bacterial composition among smokers and non-smokers have been the object of various studies.

Preber et al. did non find significant differences as for the presence of A. Actinomycetem comitans, P. Gengivalis and P. Intermedia in a group of 145 patients with advanced periodontitis (83 smokers, 62 non-smokers).

Stoltenberg et al. analyzed the presence of five different bacterial strands in a sample of 126 non-smokers and 63 smokers matched for age, sex, plaque index and presence of calculus (tartar). The analysed species were P. Gengivalis, A. Actinomycetemcomitans, P. Intermedia, Eikenella Corrodens and Fusobacterium

Nucleatum. No significant differences were present between smokers and non-smokers as for number of bacteria of each species.

In other studies, levels of microorganisms belonging to the oral microflora, such as A. Actinomycetemcomitans, P. Gengivalis, P. Intermedia, have been evaluated in smokers and non-smokers with or without a periodontal disease and even following experimental gingivitis (Lie et al.; Renvert et al.).

No significant relationship was found between the presence of these peripathogenic microorganisms and the habit of regular smoke. No relationship was also found between each single bacterial species and the various levels of inflammation.

Special note should be devoted to A. Actinomycetemcomitans, as its complete eradication is almost impossible in smokers.

Pathogenesis
Smoke-induced mechanisms in periodontal tissues may vary, as pathogenic tobacco components are numerous and have often different pathogenic activities.

Numeorus vasoactive and cytotoxic substances are found in tobacco, among these nicotine is present as the major component and is able to diffuse into epithelial cells, induce vascular alterations in the connective tissue and alter fibroblast function. A cigarette contains an average of 1 mg of nicotine. In the plasma of regular smokers, mean nicotine levels vary between 22.6-73 ng/ml while in the crevicular fluid nicotine concentrations can reach 250 ng/ml. Besides nicotine, over 4,000 toxic chemical compounds are present in tobacco; compounds mainly involved in inducing damage to the human body may be subdivided in solid, particulate and gassous ones. Solid compounds may exert a gangliomimetic effect, e.g. nicotine, an irritant effect, e.g.phenoles or a carcinogenic one, e.g. indoles and carbazoles. Gassous compounds may have an irritant and ciliotoxic effect, e.g. acetaldehyde, isoprene, cyanide and nitric and sulphur oxides; benzene and carbon monoxide are considered as carcinogenic compounds.

In 1949, Pindborg claimed that nicotine induces a vasoconstriction in the gingival margin, therefore causing an inadequate nutritive supply and a reduced resistance to infection. However, more recent studies on animals and humans did not confirm this effect for nicotine.

Martinez-Canut et al. showed that the amount of cigarette consumption is linked to greater severity of periodontal disease. In a series of 899 patients aged 21-76 years (47.4 % non-smokers, 52.6 % smokers) several parameters were evaluated including gum recession, probing depth, level of attachment and dental motility. In this study, smokers of less than 10 cigarettes/day did not show significant differences compared to non-smokers as for levels of attachment. On the contrary, smokers of 10-20 cigarettes or more/day had an increased loss of attachment in the order of 5 and 10 %, respectively. This study suggests that the clinical effect may be linked to the amount of smoked tobacco; this and other studies did not consider the time elapsed from the onset of smoking habit. The latter parameter, in addition to the entity of tobacco consumption, is likely to influence the worse progression of periodontal disease.

In a study on 13 dogs, Johnson et al. showed that systemic (2.5 mg/kg/die) or topic (8 mg/kg/die) nicotine administration over a period of 28 days did not significantly modify the pulpar blood flow. These concentrations roughly corresponded to a daily consumption of 1.5 packets of cigarettes.

In a study of 12 volunteers aged 19-25 years, Baab et al. found that cigarette smoke caused an increase, rather than a reduction, of the blood flow at the gingival margin level.The hypothesis that smoke alters an already compromised gum blood flow is based on the evidence that nicotine, or other tobacco components, may have a toxic effect on specific cellular functions.

A model for the pathogenesis of periodontal disease in smokers might be identified in a defective metabolism of soft tissue, with subsequent alteration of tissue turnover, healing and maintenance of periodontal attachment.

Hanes et al. demostrated that cultured human gum fibroblasts bind to and rapidly accumulate nicotine through a non-specific mechanism, which determines high intracellular levels of nicotine. The autors hypothesized that the intracellular presence of nicotine may alter normal cellular processes, such as collagen and protein synthesis, resulting in an alteration of healing mechanisms.

In cultured fibroblasts treated with 35 nmol/ml of nicotine, a reduced production of type III collagen was showed by Chamson et al.

Other fibroblast lines were used by Raulin et al. to investigate changes relative to morphology and substrate attachment after cellular exposition to nicotine. The latter was used at 25-400 ng/ml, which correspond or are superior to the concentration present in the plasma of regular smokers. Even at the lowest concentrations, cells showed under the light microscope a loss of the alignment that is normally found in cultured fibroblast monolayers; moreover, they appared disorganized and frequently multilayered.

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