Influence of hydrogen ion concentration (pH) of plaque
It is generally accepted that enamel caries is the result of a disturbance in the equilibrium between enamel hydroxyapatite and the calcium and phosphate ion concentrations of the dental plaque covering the enamel surface. At neutral pH, plaque seems to be supersaturated with these ions. A fall in pH, however, caused by intraplaque bacterial fermentation of carbohydrates, leads to a shift in the equilibrium of concentrations and to dissolution of enamel. The “critical pH” for enamel dissolution ranges from 4.5 to 5.5, depending on such conditions as the presence of fluoride in the plaque and enamel crystal fluids.
Because dental caries is a multifactorial disease, many factors influence the pH of plaque:
1. The amount, thickness, age, site, and composition of the plaque
2. The amount, concentration, composition, clearance time, and permeability into the plaque of fermentable carbohydrates in retentive microenvironments of the dentition, and in saliva and gingival exudate
3. The amount and quality of saliva, as well as its access to and ability to permeate the plaque
4. The concentration of fluoride, calcium, and phosphate ions in the plaque If the acidogenic theory of caries etiology is accepted, measurement of plaque pH before, during, and after a food is eaten should be a guide to its cariogenic potential.
As a basis for counseling patients on the potential cariogenicity of their diet, the acidogenicicty of various foods, drinks, and meal patterns can be compared under standardized conditions. Although acidogenicity is measured, not cariogenicity, there should be a strong correlation between the two, modified only by the possible presence of protective factors, such as fluoride, which may protect the enamel against dissolution, even at low pH.
Measurement of pH
Three main methods have been used for measuring plaque pH. The original method, still in use, is the scraping, or harvesting, method developed by Fosdick et al (1941) and subsequently used in Sweden (Frostell, 1969), the United States (Edgar et al, 1975), and the United Kingdom (Rugg-Gunn et al, 1975, 1978). Small samples of plaque are obtained from representative tooth surfaces and pooled. The pH is measured in the laboratory with a pH meter.
The touch-on/microtouch method was originally developed by Stephan (1940, 1943, 1944) in his renowned “Stephan curve” experiments. Microelectrode metal probes or glass probes are inserted in plaque in situ. The method was commonly adopted and later improved by the introduction of new thin palladium oxide microelectrodes, providing increased accessibility through the entire thickness of the plaque with less disturbance. A disadvantage is that the plaque is penetrated from the outer surface, and the “true” pH between the tooth surface and the deepest part of the plaque may be altered, for example, by saliva.
The telemetric indwelling electrode method, developed by Graf and Muhlemann
(1966), is the most technologically advanced and expensive, but also the most
accurate method for measuring the true pH beneath undisturbed plaque. A glass
electrode tip is built into either the crown of an extracted tooth or a denture tooth in a
partial prosthesis, in such a way that the tip is positioned, for example, in the
approximal space. Plaque is allowed to accumulate on the tip of the electrode. Wires
or radiotransmitters can be used to relay readings from the mouth (Figs 56a, 56b, and
56c).
Figure 57 is a detail of plaque, freely accumulated over 7 days, on the tip of an
indwelling electrode inserted in the approximal surface of an extracted natural tooth
crown fixed in a partial denture. This telemetric indwelling electrode method allows
continuous readings of pH at the undisturbed glass-tooth surface-plaque interface,
even in the least accessible areas interproximally, where metal or glass touch-on
electrodes cannot be applied.
The new microelectrodes for the touch-on method have partly overcome this problem,
but will disturb the microflora each time they are inserted at the site of measurement,
with a possible effect on plaque permeability. On the other hand, microelectrodes
allow studies on large representative samples of individuals at any site in the mouth
and can be used under field conditions.
Recent comparative studies of the three different methods (for review, see Nyvad and
Fejerskov, 1996) for measuring plaque pH have indicated that the microtouch and
telemetric methods give more pronounced pH responses than does the sampling
method and are therefore more appropriate for differentiation of the acidogenic
potential of different foods. However, irrespective of the method used, the original
observations by Stephan (1944) have been confirmed: When microbial deposits are
exposed to a fermentable carbohydrate, such as sucrose, for a short period of time (1
to 2 minutes), pH falls rapidly within the ensuing minutes. The pH then gradually
rises, although not as rapidly, and the baseline level is resumed within 30 to 60
minutes. The severity and duration of the fall in pH will depend somewhat on the
developmental stage and age of the plaque covering the tooth surface.
However, when the telemetric and Stephan methods are used concurrently on the
same plaque-covered surface, the telemetric pH curve is more individualized and
sensitive than the standard Stephan curve for different food items tested in sequence.
The telemetric method is most frequently used on posterior approximal surfaces,
which, in toothbrushing populations are the most caries susceptible. As a reference, a
lingual “plaque-free” surface is used. A 10% sucrose solution is usually used as a
positive control, after the subject has chewed a piece of paraffin wax for a few
minutes. In plaque more than 3 days old, a 10% sucrose solution results in optimal pH
fall. Most of the telemetric studies have been conducted by Imfeld (1977, 1983).
Relationship of plaque location to pH
Stephan curves from approximal plaque show significant intraoral regional
differences: Mandibular plaque has a less pronounced pH response than does
maxillary plaque (Fig 58). Even within the maxilla, there are local differences in the
Stephan response, attributable partly to variations in accessibility to saliva. The lowest
pH values are recorded for anterior sites. The gradual resumption of baseline pH
values probably results from diffusion of acids out of the plaque and the neutralizing
effect of buffers within the plaque and in the salivary film covering the plaque surface
(Fejerskov et al, 1992).
Accessibility of saliva is influenced by tooth morphology and location and variations
in the flow of saliva from the different salivary glands. Access to pits and fissures and
approximal surfaces is poor, favoring plaque acidity (Kleinberg and Jenkins, 1964);
other tooth surfaces in the vicinity of these sites will be more accessible to saliva and
as a result, the plaque will be much less acidic (see Fig 11).
Some teeth, such as the mandibular incisors, are located in regions of the mouth
where saliva is abundant. The plaque on the maxillary incisors is less alkaline than the
corresponding mandibular plaque and favors the development of caries, whereas there
is a greater tendency to calculus formation on the mandibular incisors. The volume of
saliva secreted by the major salivary glands varies considerably: The greatest flow is
from the submandibular and sublingual glands, which have duct orifices in the floor
of the mouth just lingual to the mandibular incisors.
There is an important difference between the intraoral distribution of sugar ingested in
solution and that of sugar in solid foods. Sugar in solution flows over the same tooth
surfaces as the saliva and will rapidly be cleared from the oral cavity, except under
certain conditions, eg, if ingested in high concentrations or if salivary secretion is
seriously impaired. The sugar in solid foods that have to be chewed will enter pits and
fissures and be retained in approximal embrasures, the stagnation sites in the
dentition.
By using the wire telemetric method, Igarashi et al (1989) showed that, after a 1-
minute rinse with 10% sucrose solution (Fig 59), the pH was much lower in 4-day-old
approximal plaque than in the corresponding fissure plaque.
Relationship of plaque age and composition to pH
The telemetric method has been used to evaluate the influence of plaque age on pH,
following a 2-minute rinse with 10% sucrose solution. Figure 60a shows the pH fall in
2-, 3-, 5-, and 6-day-old interdental plaque in a 14-year-old boy. Irrespective of the
subject’s age, and in experiments in the same test subject over a 2-year period, it
seems that a critical fall in pH (to below 5) occurs only in 3-day-old plaque. Figure
60b shows the fall in pH in 3-day-old plaque in a 52-year-old woman, a 7-year-old
girl, and a 7-year-old boy after they rinsed with sucrose (Imfeld, 1978, 1983).
In a toothbrushing population, such mature plaque would be found, if at all, only on
the approximal surfaces of the molars and premolars. This explains why, in such a
population, these surfaces are the most susceptible to caries.
Plaque composition also may influence the pH of plaque. The fall in pH after a
sucrose rinse would be expected to be more severe in cariogenic plaque with a high
percentage of acidogenic bacteria than in noncariogenic plaque. This is illustrated in
Fig 61. In a group of 14 year olds, the fall in plaque pH (Stephan curves) after a
sucrose rinse was measured in intact occlusal surfaces, inactive occlusal carious
lesions, and active occlusal carious lesions (Fejerskov et al, 1992). The age of the
plaque, however, may also have varied from subject to subject.
Relationship of different carbohydrates and sugar concentrations to pH and
clearance time
Neff (1967) used the Stephan method for evaluation of plaque pH changes associated
with different fermentable carbohydrates. Figure 62 (a) shows the drop in pH for
lactose, glucose, maltose, fructose, and sucrose. Figure 62 (b) shows the effect of raw
starch, cooked starch, maltose, and sucrose. These experiments indicated that raw
starch can be regarded as noncariogenic. However, under certain conditions, lactose
and cooked starch may cause a drop in pH to critical values for initiation of root
caries. In cariogenic plaque, glucose, maltose, fructose, and sucrose all seem to have
the potential to cause a fall in pH to the critical value for the development of enamel
caries.
In a series of telemetric experiments, Imfeld (1978, 1983) measured the pH beneath 4-
day-old interdental plaque after 2-minute rinses with 0.025%, 1.25%, 2.5%, 5%, and
10% sucrose solutions. At the beginning and end of each session, as well as between
treatments, the acidified plaque was neutralized by salivary flow, which was
stimulated by the chewing of neutral paraffin. If very low plaque pH values were
attained by glycolysis, rinsing with a 3% carbamide solution greatly improved the
neutralization of plaque acids, through intraplaque ammonia formation. Although
carbamide is cleared from plaque very rapidly, a further paraffin chewing phase was
introduced to ensure its removal, and this always resulted in physiologic plaque pH
values.
Figure 63 shows the telemetrically recorded pH of 4-day-old interdental plaque in one
subject during and after rinsing with increasing concentrations of sucrose solutions.
The test solutions were always spit out after the subject rinsed.
Sucrose is rapidly fermented in plaque. Regardless of the concentration of sucrose,
intraplaque pH drops immediately on sucrose intake and throughout the entire 2-
minute rinsing period. The very small quantity of sucrose remaining after the 15-mL
0.025% sucrose solution has been spit out is sufficient to depress plaque pH below
5.7. Up to a certain limit (15 mL, 10%), the amount of fermentable substrate is
negatively correlated with the lowest pH value reached. Higher sucrose
concentrations do not further depress pH. This is the rationale for using a 10% sucrose
solution as a positive control in most telemetric experiments.
Figure 64 shows the falls in pH occurring on a plaque-free lingual surface and on 4-
day-old interdental plaque after rinsing with 0.1%, 0.5%, 1%, and 5% sucrose
solutions (Imfeld, 1978, 1983). Even weak sucrose solutions (2.5% to 5%) yield
suboptimal drops in pH (to the level of pH 4.2 to 4.5), well within the critical pH
range for enamel caries.
For reference, Table 7 shows the concentrations of glucose, fructose, and sucrose in
some common Swedish food products. It is clearly unrealistic to try to exclude sugar
or reduce dietary concentrations to levels low enough to eliminate the risk of inducing
critical plaque pH values in mature, cariogenic plaque. A more realistic approach to
caries prevention and control would involve:
1. Removal of dental plaque from all tooth surfaces once or twice a day, with
concurrent use of fluoride toothpaste.
2. Restriction of the total number of food intakes, including snacks, to four to six per
day and exclusion of sticky sugar-containing products: This will reduce the total daily
sugar clearance time.
In addition to the chemical composition of foods, physical and organoleptic properties
(particle size, solubility, adhesiveness, texture, and taste) are important for
cariogenicity, because they influence eating patterns and intraoral retention of foods.
The oral carbohydrate concentration and the length of time carbohydrates remain in
the mouth during and after eating are important characteristics.
Foods are eliminated during and after mastication by the flushing action of saliva and
by the activities of the masticatory muscles, tongue, lips, and cheeks. Clearance times
may be prolonged by retentive factors in the dentition (carious lesions, poor
restorations, fixed partial dentures, and removable partial dentures), by low secretion
rates, or by high viscosity of saliva. According to the telemetric method, initial oral
carbohydrate concentrations and clearance times show large individual variations
(Imfeld, 1983) (Figs 65, 66, 67, 68, and 69), and slow clearance increases caries risk.
Different foods also vary greatly in initial oral carbohydrate concentration and
clearance times. The carbohydrates in fruits with a high acid content, such as apples
and oranges (see Figs 66 and 67), vegetables, and various drinks are eliminated within
5 minutes. Sweets, such as sugar-containing chewing gum, caramels, toffees,
chocolates, and lozenges, generally result in high oral sucrose concentrations and
clearance times ranging from 40 minutes for chewing gum to 15 to 20 minutes for
other sweets.
On the other hand, concluding each meal with sugar-free fluoride chewing gum is an
excellent caries-preventive measure, particularly for high-risk xerostomic patients.
Clearance times for bread and crackers may be reduced because the rough texture
requires vigorous chewing, which stimulates a high salivary flow. The high secretion
rate of saliva induced by vigorous chewing not only has a mechanical rinsing effect
but also increases the buffering capacity of saliva, which accelerates neutralization of
plaque acids.
Increasing the contact time between dental plaque and sucrose leads to a continuously
declining interdental plaque pH, thereby increasing its cariogenicity (see, for example,
the effect of bananas in Fig 65). The effect of other products, such as some dried fruits
and cakes, is probably even greater. In marked contrast is the effect of cheese (see Fig
68).
Bananas, which are pasty and contain 15% sugar (sucrose, fructose, glucose), have the
potential to reduce the pH of 4-day-old interdental plaque to almost the same level as
rinsing with 10% sucrose solution over a prolonged period (1.5 hours); apples (10%
sugar) and oranges seem to be noncariogenic but tend to be erosive because of their
acid content (see Figs 65, 66, and 67). This tendency may be counterbalanced by the
increased salivary flow stimulated by the acids in fruit.
Relationship of eating patterns to pH
Studies of the effect of meal patterns on intraplaque acid formation have shown that
the fall in plaque pH after consumption of sugary foods may be considerably modified
by the consumption of less fermentable foods before, concurrently, or afterward.
Imfeld (1983), using the telemetric method, demonstrated the pronounced influence of
the last course of a meal on the duration of the postprandial fall in plaque pH. Eating
30 g of Camembert cheese after lunch (see Fig 68) raised the pH of 5-day-old
interdental plaque, which had fallen during the meal, but eating chocolate cream as a
dessert prolonged and exacerbated the low pH of the interdental plaque (see Fig 69).
The observation of the effect of cheese is in agreement with other studies (Schachtele
et al, 1982). Animal studies have shown that cheese reduces caries incidence in rats
(Edgar et al, 1981). Eating cheese not only stimulates the flow of saliva but also
releases calcium and phosphate, which enhance the buffer capacity and
remineralization potential.
Relationship of sugar substitutes to pH
For thousands of years, humans have craved sweet food. Infants rapidly become
accustomed to a sweet taste, and this is sometimes acquired prenatally.
In frequently consumed snack foods such, as sweets and drinks, less fermentable and
noncariogenic sweeteners are increasingly being used as substitutes for potentially
cariogenic sugars (monosaccharides and disaccharides). These sugar substitutes are
often classified as caloric or noncaloric sweeteners. Among the caloric sugar
substitutes are the sugar alcohols (sorbitol, xylitol, and mannitol) and hydrogenated
glucose (Lycasin). Examples of common noncaloric sugar substitutes are saccharin,
cyclamate, and aspartame. Table 8 from Rugg-Gunn (1989) shows the sweetness of
different sugars and sugar substitutes relative to sucrose.
Most of the sugar substitutes have been tested by the telemetric method (Imfeld, 1983;
Imfeld and Muhlemann, 1978). Figure 70 shows the telemetric pH of 5-day-old
interdental plaque in one subject during and after rinsing with 10% aqueous solutions
of Lycasin 80/55, xylitol, sorbitol, sorbose, and sucrose.
The sugar substitutes Lycasin 80/55, xylitol, and sorbitol, and the sugar sorbose have
been declared safe for teeth according to the criteria applied by the Swiss Office of
Health. Sucrose, used as a positive control, and administered in the same way as the
sugar substitutes and sorbose, resulted in a prolonged fall in pH to below 4.5. Among
others, the longitudinal clinical Turku study (Scheinin et al, 1975) described earlier,
as well as the following chewing gum study, have shown that xylitol is noncariogenic.
All noncaloric sweeteners are also noncariogenic: They cannot be fermented at all by
the acidogenic plaque bacteria.
