Journal of Dental Research

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Flow Rates of Resting Whole and Stimulated Parotid Saliva in Relation to Age and Gender R.S. Percival, SJ Challacombe and P.D. Marsh J DENT RES 1994 73: 1416 DOI: 10.1177/00220345940730080401 The online version of this article can be found at: http://jdr.sagepub.com/content/73/8/1416

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J Dent Res 73(8):1416-1420, August, 1994

Flow Rates of Resting Whole and Stimulated Parotid Saliva in Relation to Age and Gender R.S. Percival', Sj. Challacombe, and P.D. Marshi Department of Oral Medicine and Pathology, UMDS, Guy's Hospital, London SEI 9RT, and 'Pathology Division, PHLS Centre for Applied Microbiology and Research, Porton Down, Salisbury SP4 OJG, England; *corresponding author

Abstract. Dry mouth is a common feature in the elderly, but it is not clear what proportion of incidences are related to functional disturbances and whether age per se and gender play a role. The aim of this study was to determine the effects of age and gender on salivary flow rates. The effect of age on unstimulated (resting) whole and stimulated parotid saliva flow rates was determined in 116 unmedicated, healthy individuals. The subjects were divided into four age groups: 20-39 years (group A), 40-59 years (group B), 60-79 years (group C), and 80 years and over (group D). A significant decrease in the secretion rates of unstimulated whole saliva in relation to age was observed in the study population (p < 0.001). However, the flow rates of stimulated parotid saliva were not significantly different in the four age groups. Females had significantly lower mean flow rates than males for both unstimulated (resting) whole saliva (p < 0.005) and stimulated parotid saliva (p < 0.05). In the study as a whole, significant negative correlations were found between either the DMF index (decayed, missing, and filled teeth) or the DMFS index (decayed, missing, and filled tooth surfaces) and the flow rates of unstimulated whole saliva (p < 0.02), but no relationship to stimulated parotid saliva flow rates was apparent. The results suggest that elderly subjects have no impairment in their ability to respond to sialogogues but that resting saliva rates are significantly lower than in younger individuals and may contribute to the increase in oral mucosal diseases seen in the elderly. Key words. Aging, Salivation, Gender.

Received September 20,1993; Accepted March 21,1994

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Introduction Saliva is regarded as one of the important factors in regulating oral health, with respect to both the volume produced and the constituents it contains (Mandel and Wotman, 1976). Functional disturbances of the salivary glands can cause a reduction in salivary flow and subjective dryness. These are common features in elderly people compared with younger age groups (Thorselius et al., 1988). Although numerous studies on the properties and secretion of saliva have been published, the effect of aging on saliva flow remains unclear, since conflicting observations exist in the literature. An age-related reduction in secretion rates of both resting and stimulated whole saliva (Heintze et al., 1983), a decrease in whole saliva flow rates with age (Gutman and Ben-Aryeh, 1974), and a reduction in whole and parotid saliva secretion rate with age (Yaegaki et al., 1985) have all been reported. On the other hand, no age-related decline was observed in other studies with stimulated whole salivary flow rate (Parvinen and Larmas, 1982), stimulated parotid saliva flow (Baum, 1981), or unstimulated whole and stimulated whole and parotid saliva (Gandara et al., 1985). Some of the variation in results might be due to the fact that "elderly" may be described as over 60 years of age in some studies and over 80 in others. It appears that some studies may have included subjects on systemic medications (Fure and Zickert, 1990; Narhi et al., 1992). Apart from these conflicting observations of age-related changes in flow rates, little information is available regarding the flow rate of saliva in healthy elderly individuals. In addition, very few reports are available as to gender differences in flow rate in relation to age, particularly with regard to stimulated parotid saliva (Heft and Baum, 1984; Tylenda et al., 1988). It was the aim of this

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Salivary Flow Rates, Age, and Gender

J Dent Res 73(8) 1994

study to determine whether there are age-dependent changes in salivary flow rates of resting whole and stimulated parotid saliva in a healthy elderly population.

Materials and methods Study population One hundred and sixteen healthy unmedicated subjects were selected to take part in this study and were divided among the following four groups according to their age: group A, 20-39 years (mean age, 26.7 years ± 1.06, n = 29,17 males and 12 females); group B, 40-59 years (mean age, 50.4 years + 1.08, n = 30, 10 males and 20 females); group C, 60-79 years (mean age, 71.7 years + 1.07, n = 28,16 males and 12 females); and group D, 2 80 years (mean age, 84.03 years ± 0.610, n = 29,12 males and 17 females). The subjects in groups A and B included staff and patients of Guy's Dental Hospital London, who were attending for routine dental examinations. Groups C and D were mainly comprised of healthy elderly subjects, of no particular social group, obtained from a unique college (Morden College, Blackheath, London) which was a mixture of houses, flats, and more sheltered accommodation. Subject to infirmity, these subjects also had normal lifestyles outside the residence and formed an ideal population for study. Collection of saliva samples All samples were taken between the hours of 9 and 11 a.m. Unstimulated whole saliva was collected from all subjects by direct expectoration into a sterile container over a period of 10 min so that the flow rate could be calculated. Parotid saliva flow was stimulated with 2% citric acid, added dropwise to the anterior third of the tongue, and Lashley cups (Lashley, 1916) were used to collect parotid saliva over a period of 10 min for the determination of flow rate, as previously described (Challacombe, 1976). A total of 1 mL of citric acid was applied to the tongue at the beginning of the period, and after 5 min, suction was applied with a plastic syringe via rubber tubing to the Lashley cup. This method was selected since it has been previously found to give very reproducible results when 44 subjects were re-assessed after an interval of 9 months (correlation coefficient = 0.732) and could also be considered to be more biologically relevant than maximal stimulation (Challacombe, 1980). The flow rates of resting whole and stimulated parotid saliva were measured by volume and expressed as mL/min and mL/min/gland, respectively. Clinical assessment All study participants were clinically examined for oral health and DMF (decayed, missing, and filled teeth) and DMFS (decayed, missing, and filled tooth surfaces) indices. They were also interviewed about their dental history and frequency of attendance at dental clinics. The study

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population satisfied the following requirements for inclusion within this and previous studies on microbiology of plaque and saliva (Percival et al., 1991; Marsh et al., 1992): (a) the presence of a minimum number of teeth (seven) including one molar; (b) the absence of active oral disease; (c) no history of antimicrobial therapy or other drug treatment, including immunosuppressives, diuretics, antihypertensives, or antidepressants within the previous six months; and (d) no history of diabetes. All subjects in groups C and D had received regular medical checks, and routine hematological investigations were performed. The mean number of remaining teeth per group decreased with age, while the mean DMF and DMFS increased (Table 1).

Statistical analysis Data are expressed as mean ± SEM. Differences among means were analyzed by ANOVA for statistical significance. Linear regressions were carried out on the results, assuming a normal distribution of each parameter, and the correlation coefficients were determined.

Results The mean hemoglobin concentrations of subjects in groups C and D were within the normal range and were not significantly different from those in the younger age groups, indicating no gross latent disease in the elderly. Table 1 shows the mean DMF, DMFS, and the number of remaining teeth of all the participants in the four age groups. The lowest values of DMF and DMFS were in the youngest age group (A), and significantly (p < 0.001) higher values were detected for both DMF and DMFS scores in the elderly subjects (groups C and D). No significant correlation between salivary flow rates (resting whole and stimulated parotid) and the scores of DMF and DMFS was observed in the four individual age groups (Table 2). However, in the overall series, the resting whole saliva showed a significant negative correlation with DMF and DMFS scores (r = -0.204 and -0.233; p < 0.05), but no significant relationship to stimulated parotid saliva was apparent. A comparison of the mean salivary flow rates (whole and parotid) in each age group revealed that the mean flow rate of unstimulated (resting) whole saliva in the older age groups (B, C, and D) was significantly lower than that of the youngest age group (A). The mean flow rate in the oldest age group (D) was significantly less than those in the other three groups (p < 0.001; Fig. 1). In contrast, no age-related decline in the mean value of stimulated parotid saliva was observed (Fig. 1). A significant negative correlation (r = -0.398; p < 0.001) was found between the flow rate of resting whole saliva and the age of all participants, but no significant correlation between stimulated parotid saliva flow rate and age was observed (r = -0.024). There were no significant

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Percivalet al .

j Dcti I Rcs 73(8) 1994

0.80

0.80

0.60

0.60

C:

.E E

0.40

0.400

0.20 0.00

0.00

20-39

40-59

60-79 years

20-39

80+

Figure 1. Flow rates of unstimulated (resting) whole saliva and stimulated parotid saliva in four age groups Data are reported as the mean + SEM and expressed as mL /min/gland for parotid saliva. significantly (p < 0.001) less than the 20-39-year group. - whole saliva parotid saliva

n

within-group correlations between age and flow rates. Gender-based differences in unstimulated whole saliva flow rates are presented in Fig. 2 for all age groups. Within each age group, females had lower mean flow rates than males, but these differences were statistically significant only in the oldest age group (D, p < 0.02). The value in this group was significantly lower than that for females in the other three groups (p < 0.01), and overall, the mean flow rate of 0.33 mL /mm + 0.03 was significantly less than that in

B

0.80

0.0 0.60

40-59

60-79 years

80+

Figure 2. Unstimulated (resting) whole saliva I-low rates Comparison between males and females in four age groups Data are reported as the mean + SEM. significantly (p < 0.02) lower than in males. 0X x

X

1.00

*

0.20

males' whole saliva flow rate females' whole saliva flow rate

males (0.50 + 0.04, p < 0.005). For males, the mean whole saliva flow rate in group D was significantly lower than that in group A (p < 0.001) but not in groups B or C, and both males and females showed a decrease in flow rate with age (Fig. 2). The relationship between gender and salivary low rate of stimulated parotid saliva is shown in Fig. 3. No significant differences between males and females in the individual age groups were found, but overall, the mean flow rate in females of 0.45 Tl./min + 0.04 was significantly lower than that of males (0.59 + 0.06, p < 0.05). The mean stimulated parotid flow rates for either males or females did not appear to be diminished with age (Fig. 3).

Discussion

The results of this study have demonstrated that the flow rate of unstimulated (resting) whole saliva is related to age and was significantly diminished in unmedicated healthy elderly subjects of 80 years old or more when compared with the younger age groups. This result is in agreemnent 0.00 with those of previous studies where a significant reduction 80+ 40-59 60-79 20-39 in flow rate of unstimulated whole saliva with age has becii years reported (Gutman and Ben-Aryeh, 1974; Ben-Aryeh et al, 1984; Navazesh et al., 1992) but not with others (Ilarvinen and Larmas, 1982; Gandara et al, 1985). With respect to the Figure 3. Stimulated parotid saliva flow rates Comparison between males and females in four age groups Data are reported as parotid saliva flow rate, no age-related reduction in the the mean + SEM. stimulated secretion rate was detected. This agrees with other investigators (Baum, 1981; Heft and Baum, 1984; males' parotid saliva flow rate Gandara et al., 1985) who have reported that the stimulated parotid saliva flow did not diminish with increased age in females' parotid saliva flow rate Downloaded from jdr.sagepub.com by guest on July 13, 2011 Forhealthy personal use only. No other uses without permission. The individuals. controversy in the earlier studies

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Salivary Flow Rates, Age, and Gender

j Dent Res 73(8) 1994

Table 1. Clinical assessment of all subjects showing mean DMF, DMFS indices, and number of remaining teeth Age Groups A (20-39) B (40-59) C (60-79) D (80 +) a

No. of Subjects

DMF

DMFS

No. of Remaining Teeth

29 30 28 29

9.1 + 4.7a 16.9 + 5.8 18.3 + 5.9 19.6 + 5.5

19.6 + 13.8 44.7 + 21.5 64.6 + 30.1 67.0 + 23.6

27 + 1.9 23 + 6.5 15 + 8.2 13 + 6.8

Numbers are means +±1 standard deviation.

regarding the effect of age on salivary flow rates may have been partly due to differences in experimental design, such as comparison of institutionalized subjects with noninstitutionalized controls. Few studies have included truly elderly subjects, and the correct choice of representative age range may be important. In an earlier study (Ben-Aryeh et al., 1986), 60 years was regarded as representative of old age, whereas in this study healthy subjects of over 80 years of age were included. Earlier work by Scott (1977) has shown age-related histologic changes in structure of human submandibular gland. Other workers (Pedersen et al., 1985) have reported an age-related diminution of both unstimulated and stimulated submandibular salivary f low rates. In our study, submandibular flow rates were not examined. Age-related changes of flow rates of unstimulated and stimulated labial glands have also been reported (Gandara et al., 1985; Smith et al., 1992), which may have contributed to the observed reduction in resting whole saliva flow rate noted in our study. Our findings that females had lower secretion rates of unstimulated (resting) whole and stimulated parotid saliva compared with males is in agreement with other reported results for whole saliva (Parvinen and Larmas, 1981; Thorselius et al., 1988; Fure and Zickert, 1990). With regard to stimulated parotid saliva, gender differences appear to be less marked, and our results showing a significantly greater flow in males than in females are in contrast to the results of both Heft and Baum (1984) and Ben-Aryeh et al. (1984), who did not find significant differences. This may be related to our taking samples of stimulated parotid saliva over 10 min rather than 5 min, which appears to give more reproducible results (Challacombe, 1976). These differences between the

sexes have been explained on the basis of female salivary glands being smaller than those of males (Ericson, 1970; Scott, 1975). Another factor contributing to this reduction of flow rate might be hormonal status. Women of post-menopausal age have been reported to have decreased salivary flow rates (Parvinen and Larmas, 1982), but this loss of estrogens would not be sufficient to account for reduced flow in females of all age groups, and the significantly lower values in group D females (80 years and over) suggest that age is a more important factor. In the present study, the changes in flow rate of whole saliva were directly related to age, but no age-related changes were found with parotid saliva, which indicates that healthy elderly individuals are capable of responding to stimulation and producing amounts of saliva comparable with that produced in younger individuals. In this study, the method of stimulation of parotid flow was submaximal, which has been found to be more reproducible than maximal stimulation (Challacombe, 1976) and could also be considered as more biologically relevant. In studies of this type, careful consideration should be given to the interpretation of the results if medicated individuals are included, since many medications have been shown to have a marked effect on salivary flow rates (Narhi et al., 1992). In the current study, subjects were carefully selected to exclude any effects of medication or ill health, and thus the differences in flow rates reported appear to be genuinely related to age and gender. The negative correlation between salivary flow rate and DMF in the series as a whole is consistent with previous findings in younger individuals (Challacombe, 1976) and suggests that the volume of saliva produced is an important

Table 2. Correlations between flow rates of resting whole and stimulated parotid saliva and DMF, DMFS indices

Parotid Saliva

Whole Saliva Age Groups A (20-39) B (40-59) C (60-79) D (80 +)

All subjects

No. of Subjects

DMF

DMFS

DMF

DMFS

-0.031 -0.137 0.125 0.121 29 0.118 0.086 -0.142 -0.176 30 -0.299 -0.358 0.139 -0.229 28 0.221 0.198 0.175 -0.256 29 -0.105 -0.159 -0.233a -0.204a 116 J-

Figures shown are correlation coefficients. a p < 0.05.

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jDentRes73(8)1994

Percival et al.

factor in the maintenance of oral health. It would be of interest further to substantiate the relationship between DMF and flow rate by examining a larger number of elderly individuals in group D, where the negative correlation within the group (-0.256) did not reach statistical significance. The results of this study suggest that elderly subjects have no impairment in their ability to respond to sialogogues but that resting saliva flow rates are significantly lower than in younger individuals and may reflect lack of muscular or masticatory stimulation. Since impairment of salivary secretions may make a significant contribution to the increased prevalence of oral mucosal diseases in the elderly population, a simple preventive and therapeutic measure may be to stimulate salivary flow.

Acknowledgments This research was supported by a grant from the Hayward Foundation, London. We would like to thank Mr. N. Girdler, Miss S. Van Oudgaarden, and Miss Y. Essani for collecting the samples, and the Trustees, staff, and residents of Morden College, Blackheath, London, for their help and co-operation throughout the study.

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salivary flow rate in individuals of different ages.J Dent Res 63:1182-1185. Heintze U, Birkhed D, Bjorn H (1983). Secretion rate and buffer effect of resting and stimulated whole saliva as a function of age and sex. Swed DentJ 7:227-238. Lashley KS (1916). Reflex secretion of the parotid gland. J Exp Psychol 1:461-474. Mandel ID, Wotman S (1976). The salivary secretions in health and disease. Oral Sci Rev 4:25-47. Marsh PD, Percival RS, Challacombe SJ (1992). The influence of denture-wearing and age on the oral microflora. J Dent Res 71:1374-1381. Narhi TO, Heurman JH, Ainamo A, Nevalainen JM, SchmidtKaunisaho KG, Siukosaari P, et al. (1992). Association between salivary flow rate and the use of systemic medication among 76-, 81-, and 86- year-old inhabitants in Helsinki, Finland.J Dent Res 71:1875-1880. Navazesh M, Mulligan RA, Kipnis V, Denny PA, Denny PC (1992). Comparison of whole saliva flow rates and mucin concentrations in healthy Caucasian young and aged adults. J Dent Res 71:1275-1278. Parvinen T, Larmas M (1981). The relation of stimulated salivary flow rate and pH to lactobacillus and yeast concentrations in saliva.J Dent Res 60:1929-1935. Parvinen T, Larmas M (1982). Age dependency of stimulated salivary flow rate, pH and lactobacillus and yeast concentrations.J Dent Res 61:1052-1055. Pedersen W, Schubert M, Izutsu K, Mersai T, Truelove E (1985). Agedependent decrease in human submandibular gland flow rates as measured under resting and post-stimulation conditions.J Dent Res 64:822-825. Percival RS, Challacombe SJ, Marsh PD (1991). Age-related microbiological changes in the salivary and plaque microflora of healthy adults.J Med Micro biol 35:5-11. Scott J (1975). Age, sex and contralateral differences in the volumes of human submandibular salivary glands. Arch Oral Biol 20:885-887. Scott J (1977). Quantitative age changes in the histological structure of human submandibular salivary glands. Arch Oral Biol 22:221-227. Smith DJ,Joshipura K, Kent R, Taubman MA (1992). Effect of age on immunoglobulin content and volume of human labial gland saliva.J Dent Res 71:1891-1894. Thorselius 1, Emilson CG, Osterberg T (1988). Salivary conditions and drug consumption in older age groups of elderly Swedish individuals. Gerodontics 4:66-70. Tylenda CA, Ship JA, Fox PC, Baum BJ (1988). Evaluation of submandibular salivary flow rate in different age groups.J Dent Res 67:1225-1228. Yaegaki K, Ogura R, Kameyama T, Sujaku C (1985). Biochemical diagnosis of reduced salivary gland function. IntJ Oral Surg 14:47-49.

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