Smoking, saliva and salivation

J. Dent.

14

Smoking,

1988; 16: 14-l 7

saliva and salivation

I. D. M. Macgregor Department KEY WORDS:

J. Dent

1988;

of Operative Smoking,

16:

14-l

Dentistry

Dental

School,

Newcastle

upon Tyne

Saliva, Salivation

7 (Received

29

October

1986;

reviewed

2 January

1987;

accepted

1 June

1987)

ABSTRACT

Previous reports in the literature indicate that smoking is associated with increasedplaque accumulation and mineralization. These consequences of smoking may be due to an effect of tobacco smoke on the properties of saliva. This review presents evidence that smoking increases salivary flow rate and calcium concentration, and tends to produce stimulated saliva of a relatively high pH which may favour the mineralization of plaque in smokers. Smoking does not appear to alter the rate of plaque development; the most likely reason for increased plaque accumulation in smoking being inadequate oral hygiene.

INTRODUCTION Previous epidemiological studies have established that people who smoke tobacco accumulate more dental plaque and have more calculus deposits on their teeth than non-smokers (Macgregor, 1984). These findings may in part be explained by the observations that oral hygiene practices are less thorough in smokers than in non-smokers (Macgregor, 1984, 1985; Macgregor and Rugg-Gunn, 1984; Macgregor and Balding, 1987), but might also be due to an effect of tobacco smoke on the properties of saliva and the mineralization of plaque. The calcium phosphates found in supragingival calculus are mostly derived from the saliva. The organic components of calculus and plaque matrix are similar (Silverman and Kleinberg, 1967) and arise from saliva, associated bacteria, dietary components and probably gingival fluid exudate. From clinical studies, it is evident that calculus formation is normally preceded by plaque formation (Lindhe, 1983), the soft accumulations serving as a matrix for the subsequent mineralization of the deposit. However, animal studies have shown that calculus can form by calcification of an organic matrix in the absence of a microbial plaque (Baer and Newton, 1959), and clinically there is little correlation between soft and mineralized dental deposits. Thus the factors which influence the formation and development of microbial plaque appear to be quite independent from those factors which initiate the nucleation and regulate the growth of crystallites in the organic matrix. 0

1988

Butterworth

& Co Publishers Ltd.

0300-5712/88/010014-04

$03.00

This article aims to review the effects of smoking on salivary secretion, and attempts to assess the potential of these effects to increase the formation of plaque and calculus in habitual smokers. Consideration is given to the pharmacology of tobacco smoke and its effects on the flow-rate, chemical composition and physicochemical properties of saliva.

PHARMACOLOGY

OF TOBACCO

SMOKE

The smoke from burning tobacco consists of two phases: gaseous and particulate. The gas contains many substances, including carbon dioxide and up to 5 per cent carbon monoxide heavily admixed with oxygen and nitrogen from the air (Wynder and Hoffmann, 1967). The particulate phase consists of liquid droplets and, in cigarette smoke, solid submicroscopic particles with diameters ranging between 18 rnp and 1.6 p (DallaValle et al., 1954; Kahler and Lloyd, 1957; Harris, 1960). In cigar smoke the solid particles are even smaller and are arranged around large central droplets (Kahler and Lloyd, 1957). Many of the constituents of tobacco smoke exist in a distribution equilibrium between the two phases. Some of these constituents occur in concentrations judged to be hazardous to health (US Department of Health Education and Welfare, 1976). Among the hundreds of compounds identified in tobacco smoke, the evidence suggests that it is nicotine which induces dependence

Macgregor:

(Kumar and Lader, 198 1). Nicotine has actions on almost every organ of the body. The pharmacology and toxicology of nicotine, and the adverse effects of smoking on health have been amply documented elsewhere (Larson et al., 1961; Royal College of Physicians, 1977, 1983). Salivary secretion is under neural control and is regulated by both the sympathetic and parasympathetic systems. Acetylcholine is thought to increase blood flow and cell permeability, and ‘set in train’ those changes which lead to secretion. Nicotine mimics the action of acetylcholine on autonomic ganglia, initially stimulating and subsequently preventing ganglionic transmission by a competitive type of blockade of acetylcholine. There is also evidence that nicotine acts directly on blood vessels to produce vasoconstriction (Larson et al., 196 1). Hence, the effect of nicotine in tobacco smoke on salivary secretion, which does not appear to have been studied in man, is difficult to predict. Subcutaneous injection of nicotine does not stimulate salivation in smokers or nonsmokers (Larson et al., 1961).

EFFECTS OF SMOKING FLOW RATE

ON SALIVARY

The observation that smoking increases salivary flow rate was first made by Murray in 1776 and has since been confirmed by other investigators. Winsor (1932) recorded the rate of parotid salivary flow in five smokers and five non-smokers, who each smoked a cigarette for 5 min. A marked increase in flow rate occurred in each subject during the smoking period, which continued to a lesser extent during the succeeding 5 min. During the next 25 min increased secretion continued in the smokers, but there was a marked diminution below resting level in the non-smokers. Winsor and Richard (1935) recorded a marked increase in parotid secretion in three non-smokers when they smoked cigarettes. In both of Winsor’s studies, subjects were requested to inhale. Pikielna et al. (1968) found, in 50 smokers, that ‘normal’ cigarette smoking, which was not defined further, increased resting levels of parotid flow rate by between 1.5 and 2.8 times. Pangborn and Sharon ( 197 1) reported a marked increase in parotid flow rate in eight smokers and eight non-smokers; they did not permit their subjects to inhale. Schnedorf and Ivy (1939) collected whole-mouth saliva from 15 smokers and five non-smokers for 15-min periods before, during and after smoking two or three cigarettes, but did not report whether their subjects inhaled. Salivary flow rate increased in all but two of their subjects, both smokers. Overall flow rate during smoking was double that observed before and following smoking. Pangborn and Sharon ( 197 1) also showed that when cigarettes are smoked through a filter assembly, which traps the particulate matter and allows only the gases to enter the mouth, the rate of salivary secretion is unaffected. This suggests that the salivation caused by smoking is a reflex phenomena produced by irritant

Smoking,

saliva and salivation

15

particulate matter in the smoke. Therefore pipe smokers might be expected to salivate more because they circulate the smoke around the mouth, whereas cigarette smoke tends to be inhaled. Moreover, the smoking cycle is much longer in pipe smokers than in cigarette smokers. Pipe smokers might also salivate simply because they grip the pipe-stem between the teeth. These factors do not appear to have been investigated, but pipe smokers do accumulate more supragingival calculus when compared to cigarette smokers (Frandsen and Pindborg, 1949).

EFFECTS OF SMOKING OF SALIVA Chemical

ON PROPERTIES

composition

An increase in parotid salivary flow has been shown to increase the pH and calcium concentration of parotid saliva (Jenkins, 1978), and to produce changes which favour the precipitation of calcium phosphate (Gron, 1973). A temporary increase in the calcium concentration of saliva, following smoking, was reported in 7 out of 10 cases studied by Strauss and Fockeler (1939). These authors also reported an increase in salivary potassium concentration in 5 out of 10 cases, and an increase in the salivary phosphate concentration in 10 out of 12 cases. However, the methods of estimating the concentrations of these components were not described, and by present-day standards, particularly in respect of calcium estimation, must be considered as comparatively crude. Macgregor and Edgar (1986) also described a trend towards raised calcium concentration in fresh saliva in smokers immediately after smoking a cigarette. The difference between smokers and non-smokers was statistically significant in one ofthree studies of 12 smokers and 12 non-smokers. Macgregor and Edgar (1986) also observed that salivary calcium concentration was significantly lowered after incubation of both smokers’ and non-smokers’ saliva for 24 h at 37°C. This reduction was greater in smokers than in non-smokers, although not to a significant extent. Phosphate concentrations did not show any variation with tobacco consumption and, unlike calcium concentration, did not show any significant fall after incubation. Dogon et al. (197 1) collected parotid secretion, by uniform stimulation, from 13 smokers and 12 non-smokers, every 4 h for 24 h. They found that the calcium concentration of the secretion was significantly lower, and the potassium concentration higher, in the smokers than in the non-smokers. Their finding of lower calcium concentrations in saliva at specific time-intervals does not necessarily conflict with the reports of raised calcium concentration in smokers (Strauss and Fockeler, 1939; Macgregor and Edgar, 1986) because sampling was not carried out immediately after smoking. Smoking may therefore increase the mineralizing potential of saliva. This is compatible with the finding of

16

J. Dent. 1988;

16: No. 1

raised calcium concentration in plaque in heavy smokers, compared with non-smokers (Macgregor et al., 1985), although clinical studies indicate that smoking per se does not increase the rate of plaque growth (Bastiaan and Waite, 1978; Macgregor et al., 1985). Moreover, smoking appears to have no effect on the rate of salivary precipitation (Macgregor and Edgar, 1986). Irrespective of any increase in calcium concentration in smoker’s saliva, however, if smoking increases the salivary flow rate there will be an increase in the calcium dose during and immediately after smoking. This in itself could explain the increased mineralization in smokers. Higher thiocyanate concentrations in saliva of smokers have consistently been reported (Fischmann and Fischmann, 1948; Armenio et al., 1953; Malezewski and Bass, 1955; Courant, 1967; Dacre and Tabershaw, 1970; Dogon et al., 197 1; Tenovuo and Makinen, 1976), but the reason for this increase is not known. The only known function of thiocyanate in saliva is that of an oxidizable cofactor in the lactoperoxidase antimicrobial system; it is unlikely to play any role in the formation or mineralization of plaque.

Most of the investigations described in this review employed small numbers of subjects. However, even with larger numbers, the great variation in salivary output between individuals (Jenkins, 1978) makes the quantitative study of saliva very difficult. Nevertheless, analysis of the effects of smoking on salivary proteins might throw more light on the mechanisms of plaque mineralization in people who smoke, A further potential source of plaque minerals is the fluid arising from the gingival crevice. The effects of smoking on the flow rate and composition of this fluid are not known and would be of interest. The particulate matter in tobacco smoke might itself promote mineralization. These particles are extremely small and could conceivably act as nuclei for aggregation of protein complexes, or as ‘seeding’ agents in crystal formation.

Acknowledgements I would like to thank Professor G. N. Jenkins for helpful discussion of various points.

Salivary pH and oxidation-reduction potential Kenney et al. (1975) reported a dramatic fall in the oxidation-reduction potential (Eh) of saliva in 19 smokers and 19 non-smokers immediately after smoking one cigarette. A small but significant rise in pH following smoking has also been recorded (Manhold et al., 1968; Kenney et al., 1975). Macgregor and Edgar (1986) found a barely discernible rise in pH immediately after smoking which was not statistically significant. A rise in pH would favour mineralization of plaque, while a fall in Eh provides evidence of the powerml reducing effect of cigarette smoke.

CONCLUSIONS The increase in salivation produced by smoking may explain, at least in part, the greater amounts of supragingival calculus found in smokers. However, it seems likely that the major factor leading to increased plaque accumulation in smokers is inadequate oral hygiene. It has been shown that smokers are less efficient toothbrushers, spend less time toothbrushing, and brush their teeth less frequently than non-smokers (Macgregor, 1984; Macgregor and Rugg-Gunn, 1984; Macgregor, 1985; Macgregor and Balding, 1987). The increased amounts of calcium found in smokers’ plaque probably originates from an increase in saliva production. In smokers, increased precipitation of salivary calcium might occur as a result of increased salivary protein concentration associated with the rise in parotid flow rate (Jenkins, 1978).

References Armenio G., Laforgia P. D. and Buonsaato M. (1953) Variation in concentration of thiocyanate in relation to tobacco smoke. Chem. Abstr. 41, 8876. Baer P. N. and Newton W. L. (1959) The occurrence of periodontal disease in germ free mice. J. Dent. Res. 38, 1238. Bastiaan R. J. and Waite I. M. (1978) Effects of tobacco smoke on plaque development and gingivitis. J. Periodontol. 49, 480482. Courant P. (1967) The effect of smoking on the antilactobacillus system in saliva. Odontol. Revy. 18, 251-261. Dacre J. C. and Tabershaw I. R. (1970) Thiocyanate in saliva and sputum. Relationship to smoking and industrial exposures. Arch. Environ. Health 21, 47-49. DallaValle J. M., Orr C. and Hinkle B. L. (1954) The aggregation of aerosols. Br. J. Appl. Phys. 5, Suppl. 3, S198-S208. Dogon I. L., Amdur B. H. and Bell K. (197 1) Observations on the diurnal variation of some inorganic constituents of human saliva in smokers and non-smokers. Arch. Oral Biol. 16, 95-105. Fischmann E. J. and Fischmann A. (1948) The thiocyanate content of saliva in normal and hypertensive subjects before and after ingestion of the drug. J. Lab. Clin. Med.

33, 772-776. Frandsen A. and Pindborg J. J. (1949) Tobacco and gingivitis III. Difference in the action of cigarette and pipe smoking. J. Dent. Res. 28, 464-465. Gron P. (1973) The state of calcium and inorganic orthophosphate in human saliva. Arch. Oral Biol. 18,

1365-1378. Harris W. J. (1960) Size distribution of tobacco smoke droplets by a replica method. Nature 186, 537-538. Jenkins G. N. (1978) The Physiology and Biochemistry the Mouth, 4th edn. Oxford, Blackwell.

of

Macgregor: Smoking, saliva and salivation

Kahler H. and Lloyd B. J. (1957) The electron microscopy of tobacco smoke. J. Natl. Cancer Inst. 18, 217-219. Kenney E. B., Saxe S. R. and Bowles R. D. (1975) The effect of cigarette smoking on anaerobiosis in the oral cavity. J. Periodontol. 46, 82-85. Kumar R. and Lader M. (198 1) Nicotine and smoking. Curr. Dev. Psychopharmacol. 6, 127-164. Larson P. S., Haag H. B. and Silvette H. (196 1) Tobacco. Experimental and Clinical Studies. Baltimore, Williams and Wilkins. Lindhe J. (1983) Textbook of Clinical Pen’odontology. Copenhagen, Munksgaard, p. 114. Macgregor I. D. M. (1984) Toothbrushing efficiency in smokers and non-smokers. J. Clin. Periodontol. 11, 313-320. Macgregor I. D. M. (1985) Survey of toothbrushing habits in smokers and non-smokers. Clin. Prev. Dent. 7, (6) 27-30. Macgregor I. D. M. and Balding J. W. (1987) Toothbrushing and smoking behaviour in 14-year-old English schoolchildren. Community Dent. Health 4, 27-34. Macgregor I. D. M. and Edgar W. M. (1986) Calcium and phosphate concentrations, and precipitate formation in whole saliva from smokers and non-smokers. J. Periodont. Res. 21, 429-433. Macgregor I. D. M. and Rugg-Gunn A. J. (1984) Uninstructed toothbrushing behaviour in young adults in Community relation to cigarette smoking in Newcastle. Dent. Oral Epidemiol. 12, 358-360. Macgregor I. D. M., Edgar W. M. and Greenwood A. R. (1985) Effects of cigarette smoking on the rate of plaque formation. J. CIin. Periodontol. 12, 35-41. Malezewski F. and Bass D. E. (1955) True and apparent thiocyanate in body fluid of smokers and non-smokers. J. Appl. Physiol. 8, 289.

Correspondence should be addressed to: Dr I. D. M. Macgregor, Place, Newcastle upon Tyne NE2 4BW, UK.

Book

17

Manhold J. H., Rustogi K. N., Doyle J. L. et al. (1968) Microscopic and microrespirometer (QO,) study of the effect of cigarette smoking on human oral soft tissues. Oral Surg. 26, 567-572. Murray J. A. (1776-l 792) Nicotiana tabacum. In: Apparatus Medicaminum. Gottingen, Dieterich, pp. 464475. Pangbom R. M. and Sharon I. M. (1971) Visual deprivation and parotid response to cigarette smoking. Physiol. Behav. 6, 559-561. Pikielna N. B., Pangbom R. M. and Shannon I. L. (1968) Effect of cigarette smoking on parotid secretion. Arch. Environ. Health 17, 731-738. Royal College of Physicians (1977) Smoking or Health, 3rd edn. Tunbridge Wells, Pitman Medical. Royal College of Physicians (1983) Health or Smoking. London, Pitman. Schnedorf J. G. and Ivy A. C. (1939) The effect of tobacco smoking on the alimentary tract. An experimental study of man and animals. J.A. M.A. 112, 893-904. Silverman G. and Kleinberg I. (1967) Fractionation of human dental plaque and the characterization of its cellular and acellular components. Arch. Oral Biol. 12, 1387-1405. Strauss L. H. and Fockeler J. (1939) Uber die Einwirkungen von Tabak auf die Zahne. Z. Klin. Med. 136, 468-473. Tenovuo J. and Makinen K. K. (1976) Concentration of thiocyanate and ionizable iodine in saliva of smokers and non-smokers. J. Dent. Res. 55, 661-663. US Department of Health Education and Welfare (1976) Health Consequences of Smoking. Rockeville, Maryland. Winsor A. L. (1932) The effect of cigarette smoking on secretion. J. Gen. Psycho!. 6, 190-195. Winsor A. L. and Richard S. J. (1935) The development of tolerance for cigarettes. J. Exp. Psychol. 18, 113-120. Wynder E. L. and Hoffmann D. (1967) Tobacco and Tobacco Smoke. London, Academic, pp. 85-133.

Department

of Operative

Dentistry,

Dental

School,

Framlington

Review

Clinical Periodontology for the Dental Hygienist. Fermin A. Carranza Jr and Dorothy A. Perry. Pp. 301. 1986. Eastbourne, W. B. Saunders. Softback, f22.00. The authors are to be congratulated in condensing Glickman’s Clinical Periodontology into an attractive, well laid out and readable textbook. At f22.00 it must represent very good value for money. However, a more selective reduction of material could surely have produced a textbook of more relevance to the dental hygienists to whom it is addressed. The authors’ aim to emphasize the conceptual aspects of periodontology rather than concentrate on instrumentation, and this they have certainly achieved. The first part of the book covering aetiology and pathology is excellent, sufficiently detailed without being overpowering. My main criticism concerns the second part dealing with treatment. The essence of modern periodontal therapy lies in the team approach with the dental

hygienist playing a key role, whether in general or specialist practice or in hospital periodontal departments, but this approach gains little support here. (Virtually the only use of the word ‘hygienist’ is in the preface.) Despite 40-50 references for each chapter, excellent papers emphasizing the importance of both plaque control and professional tooth cleaning in both primary and secondary prevention are not cited. Monitoring patients’ performance in plaque control, particularly in relation to bleeding on probing, is a standard part of the hygienist’s role. Yet the excellent section on these aspects in the original has been inexplicably deleted. While not wholeheartedly recommending this textbook for hygienists in the UK, these criticisms should not detract from its value to any undergraduate, or indeed practitioner, who, wishing to obtain a comprehensive view of periodontology, looks admiringly at the original, but feels unable to afford the not inconsiderable outlay. D. E. R. Cornick