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Sheiham 2015
Sheiham 2015
research-article2015
JDRXXX10.1177/0022034515590377Journal of Dental ResearchDiet and Dental Caries
Abstract
The importance of sugars as a cause of caries is underemphasized and not prominent in preventive strategies. This is despite overwhelming
evidence of its unique role in causing a worldwide caries epidemic. Why this neglect? One reason is that researchers mistakenly
consider caries to be a multifactorial disease; they also concentrate mainly on mitigating factors, particularly fluoride. However, this
is to misunderstand that the only cause of caries is dietary sugars. These provide a substrate for cariogenic oral bacteria to flourish
and to generate enamel-demineralizing acids. Modifying factors such as fluoride and dental hygiene would not be needed if we tackled
the single cause—sugars. In this article, we demonstrate the sensitivity of cariogenesis to even very low sugars intakes. Quantitative
analyses show a log-linear dose-response relationship between the sucrose or its monosaccharide intakes and the progressive lifelong
development of caries. This results in a substantial dental health burden throughout life. Processed starches have cariogenic potential
when accompanying sucrose, but human studies do not provide unequivocal data of their cariogenicity. The long-standing failure to
identify the need for drastic national reductions in sugars intakes reflects scientific confusion partly induced by pressure from major
industrial sugar interests.
mainly generated by a selective group of bacteria (Marsh 1999, whereas added sugars usually exclude fruit juices and fruit
2003; Paes Leme et al. 2006; Takahashi and Nyvad 2011). concentrates and sometimes also honey and natural syrups.
Sucrose or its individual monosaccharide constituents together Then intrinsic sugars are those incorporated within the struc-
selectively promote mutans streptococci growth and other ture of intact grains, fruit, and vegetables, and sugars from
acidogenic and acid-tolerating species (Marsh 1999, 2003; Paes milk are those naturally present in milk and milk products. A
Leme et al. 2006; Vale et al. 2007; Paes Leme et al. 2008). Paes further term sometimes used is fermentable carbohydrate,
Leme et al. (2006) concluded that “sucrose causes major bio- which refers to free sugars, glucose polymers, fermentable oli-
chemical and physiological changes during the process of bio- gosaccharides, and highly refined starches, but this does not
film formation, which, in turn, enhance its caries-inducing mean that they are fermentable within the mouth by acid-
properties.” Sucrose is the most cariogenic dietary carbohydrate producing bacteria in the dental biofilm, given the turnover
because it is fermented by oral bacteria; it also serves as a sub- time of food within the mouth.
strate for the synthesis of extracellular and intracellular poly-
saccharides in dental plaque (Zero et al. 1986; Cury et al. 1997;
Cury et al. 2000; Bowen 2002; Paes Leme et al. 2004; Ribeiro Is Dental Caries a Multifactorial Disease?
et al. 2005; Aires et al. 2006; Paes Leme et al. 2006; Ccahuana- Dental caries is a disease that requires, above all, a single spe-
Vásquez et al. 2007). After sucrose, glucose, or fructose is cific cause: free sugars (Sheiham 1987). Nevertheless, it is fre-
ingested, the pH in biofilms falls rapidly from around neutrality quently called a multifactorial condition on the grounds that
to pH 5.0 or below due to acid production by acidogenic and the disease process also involves other carbohydrates, oral
acid-tolerant bacteria, including mutans streptococci, lactoba- microorganisms, acids, differential properties of different
cilli, and bifidobacteria, and this leads to sustained demineral- teeth, salivary flow, the role of fluoride, and, modifying the
ization of the tooth structure (Bowen et al. 1966). The low pH speed of the condition, the frequency of consumption of spe-
induced by sucrose fermentation also drives a shift in the bal- cific carbohydrates. These other linked parts of the process are
ance of resident plaque microflora by favoring bacteria that often cited as causal factors. But as a means of identifying the
preferentially grow under acidic conditions at the expense of major cause, that is highly misleading. For example, the oral
many species that are associated with sound enamel. In this acid-producing bacteria that sugars give rise to are ubiquitous
way, repeated conditions of low pH select a more cariogenic in humans in all societies; all the other factors simply modify
microflora (Marsh 1991, 1994), and the extracellular polysac- the speed of the cariogenic properties of sucrose. Without sug-
charides promote changes in the composition of the biofilm ars, the chain of causation is broken, so the disease does not
matrix (Ribeiro et al. 2005; Paes Leme et al. 2006). The biofilm occur (Sheiham 1967). So, it is clear that sugars start the pro-
formed in the presence of sucrose has low concentrations of Ca, cess and set off a causal chain; the only crucial factor that
Pi, and F, which are critical ions involved in the de- and remin- determines the caries process in practice is sugars. The other
eralization of enamel and dentine (Paes Leme et al. 2006). factors mentioned above are additional factors that alter the
Extracellular polysaccharides also promote bacterial adherence primary effect of sugars, not alternative contributors (Sheiham
to tooth surfaces (Rölla 1989) and contribute to the structural 1987; Scheutz and Poulsen 1999). Thus, to stress the multifac-
integrity of dental biofilms while increasing the porosity of the torial effects on the sugars-induced causal process muddies our
biofilm formed, thereby allowing different sugars to diffuse into understanding and misdirects policy.
the deepest parts of the biofilm, resulting in low plaque pH val- When looking for causes of pathologic states, we need to
ues due to microbial catabolism (Zero et al. 1986). identify the factors that determine whether or not the disease
develops (Rothman and Greenland 2005), and dietary sugars
are clearly the key to the major differences in caries rates that
Classifications of Sugars
have been observed across the world (Sheiham 1987, 2001;
The term sugar is generally intended to mean all “dietary sug- Moynihan and Kelly 2014; Sheiham and James 2014a, 2014b).
ars,” whether added to foods or naturally occurring (Cummings The strength of the evidence for the pivotal role of sugars in
and Stephens 2007). The term added sugars are all mono- and causing caries differs markedly from the widely held erroneous
disaccharides added to food by the manufacturer, cook, or notion that caries is a multifactorial infectious transmissible
consumer—which will therefore include white, brown, raw, disease. For example, Caufield et al. (2005) consider that “by
manufactured, corn syrups, high fructose corn syrup, and so definition, dental caries is an infectious and transmissible dis-
on, but the definition does not always include honey and natu- ease because it is caused by bacteria colonizing the tooth sur-
ral syrups (e.g., maple syrup). The term free sugars, as used by faces.” They acknowledge that refined sugars have tipped the
the WHO (2015) in its sugar report, encompasses “all mono balance from health to disease. So why call caries an infectious
and disaccharides added to food by manufacturer, cook or con- transmissible disease when the presence of these microorgan-
sumer plus those sugars naturally present in honey, syrups and isms in the mouth is ubiquitous and it is only the addition of
fruit juices and concentrates.” So the only difference between sugars that then stimulates their proliferation and adhesive
the terms added and free is that the latter includes natural fruit qualities and allows them to produce the acids required for
juices and fruit concentrates, honey, and natural syrups, dental caries?
Diet and Dental Caries 3
Clinical and Epidemiologic Studies average community sugars intakes were only 1.8 g/d, caries
of Dental Caries was rare, affecting only 2% of 13- to 19-y-old children and 7%
of those aged 30 to 39 y. By the 1960s, the islands’ sugars
A series of relatively small-scale studies have been conducted intake had increased to 50 g/d (30% energy intake [E]), and
where noncariogenic sugars have been substituted for sucrose- 17.5% of children already had caries (Holloway 1963; Fisher
containing products. In the Turku study, participants continued 1968). Similarly, Sheiham (1967) reported that only 2% of
to eat starch, and a group receiving xylitol developed very little urban and rural Nigerians of all ages had any dental caries
caries compared with the sucrose group (Scheinin et al. 1976). when their average free sugars intakes were about 2 g/d per
The Turku studies corroborate the findings from studies of person (0.4% E). Analyses from Tanzania and China, where
people with hereditary fructose intolerance (Scheinin et al. free sugars intakes were 9.08 kg/capita per year (5% E) and
1976; Newbrun et al. 1980) where those individuals with 6.9 kg/capita per year (3.8% E), respectively, the DMFT was
hereditary fructose intolerance, who cannot tolerate and abso- 0.30 in Tanzanian and 0.53 in Chinese 12-y-olds (Sheiham and
lutely avoid eating sucrose or fructose, have strikingly reduced James 2014b).
dental caries rates (Newbrun et al. 1980; Newbrun 1982). Analyses of the relation between national free sugars
However, the difficulty of undertaking single-blind, let alone intakes (often based on sugar availability data as a proxy for
double-blind, community-based randomized trials of sucrose national consumption rates) and caries prevalences during
reduction over sufficient periods to monitor dental caries World War II amplify the close correlation between sugars and
development makes it impossible to satisfy the current WHO caries (Sognnaes 1948; Takeuchi 1961; Moynihan and Kelly
assessment of the strength of evidence based on the GRADE 2014). In Iraq, there was a marked responsiveness of caries to
classification of evidence used by WHO (Balshem et al. 2011; prevailing free sugars intakes: levels of dental caries in Iraqi
WHO 2014), which relies on evidence from randomized trials children halved after United Nations sanctions reduced sugars
and coherent evidence from cohort studies. Double-blind inter- from 50 kg/capita per year (27.4% E) before sanctions to
vention studies are exceptionally difficult to undertake when 12 kg/capita per year (6.6% E) 5 y later (Jamel et al. 2004).
they involve changing a sweet component of the major macro- Meta-analyses confirmed the statistical relationship between
nutrient, namely a carbohydrate; the sucrose needs to be average sugars intakes and the prevalence of caries (Masood
replaced with some other energy-producing component, which et al. 2012; Moynihan and Kelly 2014). These then reinforced
may have different metabolic and clinical effects. Furthermore, the evidence obtained during wartime sugars rationing and
the trial participants would readily recognize the diet as being sanctions on sugars imports.
different, thereby negating the blinded requirement of a good
trial. Thus, almost all studies on sugars and caries come from
many types of investigation—cellular and molecular physio- Takeuchi’s Japan Studies
logic, clinical, and short-term unblended trials, which are then The most remarkable data on the relationship between dietary
linked with observational data rather than robust controlled sugars and caries come from the meticulous sequential annual
randomized trials (Moynihan and Kelly 2014). These labora- studies conducted in Japan by Takeuchi and colleagues
tory, physiologic, and clinical assessments by dental scientists (Takahashi 1959; Okuya 1960; Takeuchi 1961; Koike 1962;
have not managed to build a scientifically tested model of car- Sheiham and James 2014a, 2014b). Takeuchi’s studies were
ies without the pivotal role of sugars. The extensive scientific based on comprehensive national data from Japan, where
literature is now emphasizing free sugars as the primary neces- before, during, and after World War II, per capita sugars levels
sary factor in the development of dental caries based appropri- decreased from 15 kg/y (8.2% E) to 0.2 kg (0.1% E) and then
ately on the multiplicity of different types of study (Moynihan increased again to 15 kg/y over a period of 11 y. Each tooth
and Petersen 2004; Moynihan and Kelly 2014; Sheiham and was examined separately at yearly intervals in each individual.
James 2014a, 2014b). This balanced judgment, based on dif- The results of these studies showed a clear relationship between
ferent forms of evidence, was emphasized as appropriate by the average sugars intake level and dental caries specified as
the UK National Institute of Clinical Excellence (2012). It is that which had progressed to cavitation.
also important to recognize that if the presence of sugars is Takeuchi and coworkers also noted marked differences in
critical to the incidence of caries, then the prevalence of caries tooth susceptibility to caries (Takahashi 1959; Takeuchi 1961;
in a community or country will be linked to the prevailing sug- Koike 1962; Takeuchi et al. 1971). When the choice of teeth
ars intake if there is a quantitative relationship between sugars was standardized, the time since the teeth had erupted—
intake and the magnitude of the disease and if other modifying namely, the length of exposure to the prevailing diet—was also
factors do not have a major and confusing effect on the sugar- important. The cumulative effect of these processes was then
caries relationship. evident in susceptible molar teeth and the most resistant incisor
teeth, with the documented progressive development of caries
over an 8-y period following tooth eruption.
Population Studies There was no evident threshold for sugars’ effect on caries,
National analyses from low-income countries show that dental but a log-linear relationship in caries rates even for sugars
caries was very uncommon before people started consuming intakes between 2 kg/y (1.0% E) and 5 to 7.5 kg/y (2.7% to
refined sugars. Thus, in Tristan de Cunhans in 1938, when 4.1% E) in teeth erupted for 7 to 8 y. Moreover, whatever the
4 Journal of Dental Research
prevailing level of sugars intake, the actual annual accumula- about 1.5% E) in 1998 and 10.5 g/d (2% E) in 2011, the DMFT
tion of caries progressed linearly (Takeuchi 1961). These was 2.0 in 12-y-olds and 5.2 in 35- to 44-y-olds; only 3.2 sur-
unique studies emphasize the differential tooth susceptibility to faces were affected in 12-y-olds, but 14.3 were carious in 35-
caries and the importance of the posteruptive tooth age (Okuya to 44-y-olds, with 39 surfaces out of a total of 160 by 65 to
1960), so the regression lines between caries incidence and 74 y of age (Ministry of Health and Welfare 2011). These data
annual sugars consumption differed for each kind of tooth emphasize the importance of considering the adult burden of
(Takahashi 1959). Even the caries resistant upper central inci- dental disease when assessing optimum intakes of sugars.
sors had caries at sugars intakes below 5 kg/y (2.7% E), and the
susceptible molar teeth in Japan, without much fluoride at that
time, showed almost a maximum impact at sugars intakes of Impact of Fluoride on the
15 kg/y (8.2% E; Takahashi 1959). Sugars-caries Relationship
Fluoride alters the dose-response relationship between sugars
Dose-response Relationships between and caries by delaying when cavitation occurs for a given level
of sugars (Zero 2004). The widescale use of fluoride toothpaste
Sugars and Caries
explains the decline in children’s caries, yet what then becomes
The log-linear or, in arithmetic terms, curvilinear dose- evident is that caries becomes more prominent in adolescents
response relationship between free sugars and caries has been and adults (Bernabé and Sheiham 2014).
repeatedly observed (Okuya 1960; Koike 1962), even though Water fluoridation decreases caries in children, but there are
the chosen diagnostic level of caries was cavitation. Koike few studies on its effects over the life course. Such studies
(1962) found no evident threshold for sugars but a log-linear show that even when high percentages of water supplies were
increase in caries rates between <1 kg sugars/caput/y (0.05% fluoridated, the progressive increase in DMFT with age is evi-
E) and 5 to 7.5 kg sugars/caput/y (2.7% to 4.1% E) if teeth that dent, with most of the disease occurring in adults. In Australia,
have been erupted for 7 to 8 y are considered (Okuya 1960; mean numbers of DMFT and DMFS increased 10-fold from
Koike 1962). Takahashi (1959) also found a log-linear rela- the youngest to the oldest age groups (Slade et al. 2013). In
tionship (r = 0.8) between dental caries increment and sugars Ireland, with fluoridated water supplying 73% of the popula-
intakes between 0.2 kg (0.1% E) and 5 to 7.5 kg/person/y tion for >50 y, the DMFT was 1.30 in 12-y-olds and 15.0 in
(2.7% to 4.1% E) in first permanent molars that had previously 35- to 44-y-olds: the numbers of DMFT in nonfluoridated and
erupted for 7 to 8 y, with greater impacts on lower than upper fluoridated areas were 16.0 and 13.3 in 35- to 44-y-olds and
first molars and with a log-linear relation at both lower and 26.7 and 25.9 for ≥65-y-olds, respectively (Whelton et al.
higher sugars intake levels for all tooth types if 1 to 8 y of sug- 2007).
ars exposure is considered (Okuya 1960; Takeuchi 1961; Koike Despite the wide-scale use of fluoridated toothpaste and
1962). A much later Japanese study in 12-y-olds by Miyazaki consumption of fluoridated water by 66% of Americans since
and Morimoto (1996) further showed a positive log-linear cor- the 1960s, adults aged 65 to 74 y had an average DMFS of 70
relation of 0.91, with caries increasing as sugars consumption (Dye et al. 2007). Thus, although fluoride reduces caries, unac-
rose to a peak of 29 kg/y (15.9% E) in 1973. These findings ceptably high levels of caries in adults persist in all countries,
from cross-sectional surveys indicate that there was a strong even where there is wide-scale water fluoridation and the use
positive correlation ranging from 0.7 to 0.9 between free sug- of fluoridated toothpastes (Dye et al. 2007).
ars consumption and caries (Miyazaki and Morimoto 1996;
Moynihan and Kelly 2014). The frequency of sugar-sweetened
beverage consumption relating to increasing caries was noted Systematic Reviews on the Effect on Caries
in a nationally representative Finnish adult population despite of Restricting Free Sugars Intakes
the use of fluoride toothpaste (Bernabé et al. 2014). A dose- The most comprehensive systematic review ever conducted on
response relationship between frequency of sugar-sweetened sugars and caries using rigorous methods was by Moynihan
beverage consumption and caries increment was additionally and Kelly (2014), who found a large effect size for the impact
reported in Australian children (Armfeld et al. 2013). of sugars intake on dental caries. Furthermore, their analyses
indicate that dental caries progresses with age and that the
Dental Caries in Adults effects of sugars on the dentition are lifelong. Even with low
levels of caries in childhood, there were progressive increases
Most studies on the relationship between sugars and dental car- throughout the life course, and despite the protection offered
ies have been conducted in children (Moynihan and Kelly by fluoride, the causal relationship between free sugars and
2014). Yet, the majority of caries in permanent teeth occurs in dental caries remains.
adults, not children (Bernabé and Sheiham 2014), indicating
that a sugars-induced dental caries progresses throughout life
Caries Induced by Dietary Starches
(Sheiham and James 2014a, 2014b). Even in countries with
low sugars intakes, the DMFT was higher in adults than in chil- Although processed food starches in modern human diets pos-
dren. In South Korea, with sugars intakes between 7.3 g/d (i.e., sess a significant in vitro cariogenic potential, “the available
Diet and Dental Caries 5
studies with humans do not provide unequivocal data on their WHO suggests a further reduction of the intake of free sugars to
actual cariogenicity” (Lingstrom et al. 2000). People eating below 5% of total energy intake (conditional recommendation).
low-sugar, high-starch diets typically have very low levels of
caries. Chankanka et al. (2011) found a positive relationship Strong recommendations indicate that “the desirable effects
between processed starchy snacks (e.g., potato chips, tortilla of adherence to the recommendation outweigh the undesirable
chips, flavored crackers) and caries. Their findings differ from consequences” and that “the recommendation can be adopted
those by Marshall et al. (2005) on the same study population as policy in most situations.” Conditional recommendations
and with the same methods, finding that snack and daily total are made when there is less certainty “about the balance
exposures to starches and processed starch exposures were not between the benefits and harms or disadvantages of imple-
associated with caries. Chankanka and colleagues’ findings menting a recommendation” and when “policy-making will
support those by Campain et al. (2003), who used a more real- require substantial debate and involvement of various stake-
istic grouping of foods and reported that there were significant holders for translating them into action” (WHO 2014, 2015).
interactions with caries and starch. The conclusions by Rugg- Although the need to reduce sugars intakes was based on
Gunn (1993) on the relation between starches and caries are obesity and dental caries issues, the dental analyses, rather than
nevertheless still valid in that—under some circumstances the weight gain studies, allowed quantitative estimates to be
with sugars present, particularly in susceptible individuals— made—despite these analyses being previously ignored by
starch can amplify the sugars risk. Rugg-Gunn specified that 1) dental researchers, dental organizations, and educators—and
cooked staple starchy foods (e.g., rice, potatoes, bread) are of are now presented in this review.
low cariogenicity in humans; 2) the cariogenicity of uncooked
starch is very low; 3) finely ground and heat-treated starch can
induce dental caries, but the amount of caries is less than that
Sugar Industry’s Influence
caused by sugars; and 4) the addition of sugars increases the on the Policies on Sugars
cariogenicity of cooked starchy foods. The sugar, food, and drink industries protect themselves from
potentially damaging information and research suitable for
policy makers by lobbying and influencing research policy
WHO Guideline: Sugars Intake (Kearns et al. 2015). Denying evidence that sugars are harmful
for Adults and Children to health has always been at the heart of the sugar industry’s
defense. The industry’s tactic is to undermine all the scientific
The objective of the WHO (2015) guideline is to provide rec- evidence by supporting scientists who offer contrary evidence,
ommendations on intakes of free sugars to reduce risks of non- thereby creating a “controversy.” They also fudge and offer
communicable diseases in adults and children, with a focus on contrary evidence to delay any policy decisions and manipu-
the prevention and control of unhealthy weight gain and dental late governments to procrastinate (Bes-Rastrollo et al. 2013;
caries. The WHO recognized that dental diseases are the most Goldman et al. 2014). Their influence on national and interna-
prevalent noncommunicable diseases globally and that the tional committees is considerable (Kearns et al. 2015). The
treatment of dental diseases is expensive, exceeding the entire World Sugar Research Organisation, representing sugar indus-
financial resources available for the health care of children in try interests, successfully blocked the 1990 and 2003 WHO /
most lower-income countries. Food and Agriculture Organization joint committees’ recom-
The evidence for the WHO recommendations is as mendations on sugars from becoming WHO policy, as we
follows: know from personal experience and as noted by Kearns et al.
(2015). Kearns et al. also showed how the sugar industry
An analysis of cohort studies in children suggests a positive funded research on a vaccine against tooth decay with ques-
association between the level of free sugars intake and dental
tionable potential for widespread application. It influenced
caries. The evidence suggests higher rates of dental caries
policy in the US National Institute of Dental Research, which
when the level of free sugars intake is more than 10% of total
changed the proposals for the National Caries Program to
energy intake compared with it being less than 10% of total
energy intake. Additionally, a positive log-linear dose-response
exclude the proposal to restrict sugars consumption to prevent
relationship between free sugars intake and dental caries was caries (Kearns et al. 2015).
observed across all studies, at free sugars intakes well below
10 kg/person/year (i.e. <5% of total energy intake). Conclusions
The WHO generated the following recommendations for Dental caries is a diet-mediated disease. There is extensive sci-
free sugars intake in adults and children: entific evidence that free sugars are the primary necessary fac-
tor in the development of dental caries. Acid-producing
WHO recommends a reduced intake of free sugars throughout bacteria and other factors facilitate the development of dental
the lifecourse (strong recommendation). In both adults and caries, but free sugars are the necessary dietary cause of caries,
children, WHO recommends reducing the intake of free sugars with consistent evidence for a markedly sensitive log-linear
to less than 10% of total energy intake (strong recommendation). dose-response increase in caries from 0.1% sugars intake to
6 Journal of Dental Research
2% to 3%. A 10% sugars intake was noted by the WHO (2015) Dye BA, Tan S, Smith V, Lewis BG, Barker LK, Thornton-Evans G, Eke PI,
Beltrán-Aguilar ED, Horowitz AM, Li CH. 2007. Trends in oral health
as inducing high caries rates despite fluoride use in drinking status: United States, 1988–1994 and 1999–2004. Vital Health Stat.
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defects in Tristan da Cunha. Br Dent J. 125(10):447–453.
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Author Contributions subtracted science—how industry obscures science and undermines public
health policy on sugar. Center for Science and Democracy [accessed 2015
A. Sheiham, contributed to conception, design, data analysis, and Mar 10]. http://www.ucsusa.org/assets/documents/center-for-science-and-
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W.P.T. James, contributed to conception and design, critically Holloway PJ. 1963. Dental disease in Tristan de Cunha. Br Dent J. 115(1):19–
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revised the manuscript. Both authors gave final approval and Jamel H, Plasschaert A, Sheiham A. 2004. Dental caries experience and avail-
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Acknowledgments Kearns CE, Glantz SA, Schmidt LA. 2015. Sugar industry influence on the sci-
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The authors received no financial support and declare no potential Caries Program: a historical analysis of internal documents. PLoS Med.
conflicts of interest with respect to the authorship and/or publica- 12(3):e1001798.
Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJ, Marcenes W.
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