加工でんぷんスナック製品（PSSP）とう蝕：ナラティブレビュー

Abstract

Aim: The consumption of processed starch snack products (PSSPs) has become widespread, raising concerns about their overconsumption and potential impact on overweight-related diseases including dental caries. This narrative review aims to evaluate the evidence linking PSSPs and caries focusing on Japanese PSSPs.

Materials and Methods: We conducted a search in our personal libraries and updated our collection with articles published within the last 20 years that met the predetermined inclusion criteria for a systematic search. In total, we summarised 75 articles.

Results: This review outlined the structure, types, dietary sources and metabolism of starch and discussed the cariogenicity of PSSPs, along with methods for evaluating it and behavioural factors influencing dental caries, such as the frequency and timing of consumption. The cariogenicity of PSSPs was categorised into three aspects: bioavailability, retentive properties and consumption frequency. Studies have demonstrated that combinations of starch and sugar, often found in many PSSPs, exhibited a higher cariogenic potential compared with sugar alone. As dental caries is a complex condition influenced by multiple factors, all of which depend on the individual, the dietary factor itself is also multifactorial and it was divided into two main factors: product and individual related. The latter factor (i.e. how you eat) is more important. For this reason, recent changes in Japanese eating habits, with an increasing preference for PSSPs and a prevalence of unhealthy eating behaviours, may have a negative impact on oral health. In addition, marketing portrays PSSPs as convenient, tasty and quick sources of energy, occasionally adding seemingly healthy ingredients but promoting demineralisation and erosion.

Conclusion: PSSPs are associated with dental caries due to their high bioavailability, long retention on teeth and high palatability. Japanese dental hygienists need to control the caries risk comprehensively and provide patient education on how PSSPs affect overweight-related diseases including dental caries.

Translated Abstract

目的：加工でんぷんスナック製品（PSSP）の過剰摂取や，う蝕を含む過体重関連疾患への影響に懸念が高まっている。本ナラティブレビューは日本のPSSPを取り上げ，PSSPとう蝕に関するエビデンスの評価を目的とする。

対象および方法：事前設定したシステマティックサーチの包含基準を満たす過去20年以内に出版された論文で個人の蔵書を更新した。合計75の文献を要約した。

結果：本レビューでは，デンプンの構造などを概説し，PSSPのう蝕原性，評価方法，影響を及ぼす行動因子を考察した。PSSPのう蝕原性を生物学的利用能，停滞性，摂取頻度の3つに分類した。多くのPSSPにも認められるデンプンと糖の組み合わせは，糖単独より高いう蝕原性を示す。う蝕は多因子性疾患だが，食事因子自体も多因子で，それらを2要因に分けた。後者の要因（食べ方）の方が重要である。このため，最近の日本人のPSSPへの嗜好の高まりや不健康な食行動の蔓延は口腔保健に悪影響を及ぼす可能性がある。加えて，PSSPは便利で美味しく，手軽なエネルギー源として宣伝され，健康に良さそうな添加成分が，脱灰と酸蝕を促進することもある。

結論：PSSPは，高い生物学的利用能，長い歯面停滞時間，高い嗜好性により，う蝕と関連している。日本の歯科衛生士は，う蝕リスクを包括的に管理し，PSSPがう蝕を含む過体重関連疾患に影響することについて患者教育を行う必要がある。

I.  Introduction

In modern times, consuming processed starch snack products (PSSPs), such as rice crackers, potato chips (crisps), popcorn and extruded cheese puffs (Figure 1), has become widespread¹⁾. These starchy snacks often lead to overconsumption and contribute to overweight-related diseases²⁾. However, their impact on dental caries has not been extensively studied and discussed^3),4).

Figure 1.

Processed starch snack products sold in Japan.　#1: shrimp snacks, #2-3: rice crackers, #4-5: potato chips (crisps), #6: popcorn,　#7: extruded cheese puffs, #8: caramel-coated corn snacks.

Dental caries is a prevalent oral disease affecting individuals worldwide, in countries including Japan, regardless of age⁵⁾. The demineralisation of the tooth surface is primarily caused by acids produced through the bacterial fermentation of fermentable carbohydrates present in the dental plaque (i.e. dental biofilm); salivary α-amylase facilitates the cleavage of these carbohydrates⁶⁾. While the link between sugars and dental caries is well established^7),8), the relationship between food starch and caries is complex^9),10) and still the subject of debate.

A recent systematic review¹¹⁾ explored the effects of food starch on oral health outcomes, distinguishing between rapidly digestible starches (RDSs), such as processed starches, and slowly digestible starches (SDSs), such as whole grains, legumes and starchy vegetables. That systematic review found that RDS intake may significantly increase caries risk. Nevertheless, the systematic review did not clarify the cariogenicity of PSSPs mentioned above, such as the ones commonly found in Japan, Sweden and other industrialised countries. Another systematic review by Hancock et al. (2020)⁴⁾focused on the cariogenicity of processed starch and sugar, as well as behavioural factors; the authors emphasised that processed foods containing starch and sugar, even those not described as “sweet”, were associated with dental caries. These findings have important clinical implications for Japanese dental hygienists responsible for patient education.

This narrative review aims comprehensively to evaluate the evidence linking starch, mainly PSSPs, and dental caries, indicating examples of Japanese PSSPs. The review will begin with an overview of the structure, types, dietary sources and metabolism of starch. This will be followed by a discussion of how PSSPs can cause dental caries, with methods for evaluating starch cariogenicity. Additionally, potential behavioural factors influencing the relationship between PSSPs and dental caries, such as the frequency and timing of starch consumption, will be discussed. Finally, the review will focus on the Japanese context and provide potential implications of these findings for public health policy and dental practice for Japanese dental hygienists.

II.  Materials and methods

Initially, we conducted a search in our personal libraries and updated our collection with articles published within the last 20 years that met the predetermined inclusion criteria for a systematic search (see Supplements). It was conducted on 11 June 2023, with a publication date restriction starting from 1 January 2003. No language restrictions were imposed in this systematic search. The authors, whose native languages were Japanese and Swedish, were proficient in English, Danish, Norwegian and German and used translation tools (DeepL Translate and Google Translator) when needed. The number of identified articles was 87 and 24 of them met the predetermined inclusion criteria. By combining the results of our search in personal libraries, we summarised a total of 75 articles in this narrative review.

III.  Starch and its metabolism in the oral cavity

Starchy foods, including rice, bread, pasta, potatoes and cereals, are a vital component of our diet, comprising around one-third of it. Starch is a type of carbohydrate that is a glucose polymer consisting of two components, namely amylose and amylopectin. Amylose is linearly linked by α-1,4 bonds, while amylopectin is branched by α-1,4 and α-1,6 linkages. Salivary enzyme α-amylase rapidly cleaves (i.e. hydrolyses) both amylose and amylopectin in the oral cavity, breaking them down into small molecules^{12),13),14),10)}. The end products of this enzymatic hydrolysis are mostly maltose and maltotriose, but also dextrins and, to some degree, glucose, which are cariogenic sugars fermented by bacteria in the dental biofilm^15),16) (Figure 2).

Figure 2.

The enzymatic hydrolysis of starch by α-amylase.　Amylopectin and amylose make up starch. In the oral cavity, salivary enzyme α-amylase hydrolyses into smaller molecules. The end products of this enzymatic hydrolysis are maltose, maltotriose, dextrins and glucose.

The rate of starch digestion varies and is determined by both intrinsic and extrinsic factors¹⁷⁾. As a result, starches can be rapidly digested (i.e. rapidly digestible starch or RDS), slowly digested (i.e. slowly digestible starch or SDS), or only partially digested in the small intestine (i.e. resistant starch) and these different types of starch can have varying impacts on systemic and oral health¹¹⁾. PSSPs, such as rice crackers, potato chips (crisps), popcorn and extruded cheese puffs, are classified as RDS. Modern techniques such as popping, steam-flaking, or extrusion cooking are used to produce expanded snacks and crispbread-like products, which modify their structural and physical properties, affecting their susceptibility to enzymic hydrolysis by α-amylase^18),19).

IV.  Cariogenicity of PSSPs

1.  How to evaluate cariogenicity

In-situ methods have been developed to a point at which they are considered valid for assessing the cariogenicity of various foods, drinks and some oral health products²⁰⁾. By combining the in-situ model with the plaque pH methods, the cariogenicity of foods, drinks and other oral products can be evaluated. Conversely, the UK workshop group expressed apprehension that the number of laboratories with adequate staff and resources to carry out the animal (rat) model for assessing the cariogenicity of foods and diets is dwindling²⁰⁾. The “Stephan curve” is still an effective tool for evaluating the cariogenicity of starch products, as depicted in Figure 3²¹⁾. It can be concluded that “the lower the plaque pH, the higher the risk of caries”.

Figure 3.

Telemetrically recorded pH of interdental plaque in different subjects during and after the consumption of the products (potato chips (crisps) and popcorn).　PC = 3 min paraffin chewing; H₂O = 2 min water rinse; U = 2 min 0.5 ml/l (3%) urea rinse; d = days, age of plaque (cited from Imfeld (1983)²¹⁾ with permission of S. Karger AG).

2.  Three aspects contributing to cariogenicity

PSSPs have become popular worldwide between meals, resulting in a deep pH fall in the dental biofilm (Figure 3)²¹⁾. The results of epidemiological studies suggested that the intake frequency of foods rich in semi-hydrolysed starch (salty or savoury snacks, crisps and industrial bread, whether or not combined with sugar)²²⁾ and refined starch (white bread and snack crisps) were significantly associated with caries experience²³⁾.

Three aspects contributing to the cariogenicity of PSSPs are 1) their bioavailability, 2) retentive properties and 3) consumption frequency. Firstly, PSSPs have a high bioavailability in the mouth and to salivary α-amylase because of the modern techniques such as popping, steam-flaking, or extrusion cooking²⁴⁾ mentioned above. A study of four adults demonstrated that the pH in dental biofilm after bread inoculation was reported to range from 4.0 to 5.5 and after cookie inoculation from 4.3 to 5.2, suggesting that wheat starch was degraded by α-amylase and was cariogenic²⁵⁾. According to an Iranian study, the use of less refined flour in traditional Persian bread (Sangak) with a higher temperature (250-350 °C) and shorter baking time (a few minutes)²⁶⁾ resulted in a lower drop in pH within the dental biofilm compared with the flour used in modern bread (baguette)²⁷⁾.

Secondly, PSSPs are retained for a long time on the teeth (see the section “V. Behavioural factors regarding diet and dental caries”). High-starch snack foods tend to stay longer on the teeth compared with high-sucrose, low-starch foods, even though the consumer's perception of stickiness is low²⁸⁾. A recent study comparing the total carbohydrate content of salivary expectorants in children after consuming different processed foods ensured a lower rate of salivary clearance with a high starch content, such as cornflakes and potato chips (crisps), than biscuits and cake²⁹⁾.

The salivary flow rate is a significant factor when considering food retention. Potato chips (crisps), sugar-free cheese puffs and sweetened crackers resulted in a lower plaque pH and a longer oral retention time when consumed at a reduced salivary secretion rate compared with normal salivary flow (Figure 4)³⁰⁾. This observation is of great clinical significance for older adults who frequently encounter xerostomia (dry mouth) and run the risk of root surface exposure¹⁰⁾.Thirdly, PSSPs can be eaten frequently due to their high palatability. Young people in particular often eat snacks while watching movies, playing computer games and so on, as shown in a Finnish study³¹⁾. In Sweden, the consumption of snack foods such as crisps and candies increased by 367% from 1960 to 2010, although the consumption of starches, including flours and pastas, declined by 6%³²⁾. The authors suggest that the increased consumption of ultra-processed foods (UPFs) may be due to their highly palatable nature, which is achieved by adding high levels of sugar, salt, fat and other additives. UPFs include PSSPs and other foods that undergo multiple processes, including extrusion, melding and milling, and contain many added ingredients, making them highly manipulated³³⁾. The convenience and low cost of UPFs may contribute to their popularity as well³²⁾. Additionally, it is noteworthy that the consumption of some UPFs or PSSPs as comfort foods increases during stressful situations³⁴⁾. A recent systematic review and meta-analysis showed a strong association between UPFs and dental caries³⁵⁾. The authors make an important point that, despite sucrose being extensively studied in relation to caries, there is an ongoing discussion among researchers about the potential impact of processed starches that tend to remain on the teeth and are commonly found in UPFs and that alternative carbohydrates may have a significant role to play.

Figure 4.

Changes in pH of human dental plaque after consumption of 5 g potato chips (crisps), cheese doodles, or crackers and after a mouthrinse with 10 ml of 5% starch and 5% sucrose at normal (to the left) and low (to the right) salivary secretion rates.　Mean values for 10 subjects. pH 6.5 is indicated as a broken line (cited by Lingström (1993)³⁰⁾ with permission of Acta Odontologica Scandinavica).

3.  Starch combined with sucrose

The cariogenicity of starchy food, even PSSPs, is lower than that of sucrose^36),37),3). Even if they are less cariogenic than sucrose, the difference between PSSPs and sucrose may be smaller than many patients believe, if eaten frequently. Furthermore, caution should be exercised when starchy foods are combined with sucrose.

In microbiological tests, the presence of both sucrose and starch impacted the production of exopolysaccharides in lactic acid bacteria³⁸⁾ and the genes and molecules of Streptococcus mutans³⁹⁾ during the process of forming a biofilm, although other studies did not find a statistical difference between starch combined with sucrose and sucrose alone^40),41). An early rat study showed that, when sucrose powder and wheat starch were consumed alternately, the cariogenicity was comparable to that of sucrose meals; in addition, a 1:1 mixture of cooked wheat starch and sucrose powder was found to be as cariogenic as, or more cariogenic than, sucrose meals⁴²⁾. More recently, a Brazilian research group examined the cariogenicity of food products containing a mixture of starch and sucrose (0.9% NaCl, 1% starch, 10% sucrose and a combination of 1% starch and 10% sucrose) exposed on bovine root dentine slabs; they found that a combination of starch and sucrose was more cariogenic for root dentine slabs than sucrose alone⁴³⁾.

Other in-vitro, in-situ and in-vivo studies have also demonstrated that combinations of starch and sugar are more cariogenic than sugar alone^44),45),46). This is clinically relevant, as people often consume baked goods, such as cookies, pastries and cakes, which contain both these carbohydrates. Additionally, caution should be taken with some PSSPs that are coated with sugar, which are not as sweet as those baked goods (Table 1, #8).

Table 1.

Product- and individual-related dietary factors of importance for dental caries (cited from Birkhed (1990)^47）).

V.  Behavioural factors regarding diet and dental caries

This section is a summary of Birkhed (1990)⁴⁷⁾.

1.  WHAT and HOW you eat

There is overwhelming evidence that the frequent ingestion of fermentable carbohydrates (i.e. starch and sugars) is associated with the high prevalence of dental caries, even if caries is a multifactorial disease. The “diet” itself is also multifactorial and can be divided into two main factors: product and individual related (Table 1)⁴⁷⁾. For this reason, both WHAT and HOW you eat are essential for dental caries, but they are, to some extent, independent of one another and HOW frequently you eat is more important for caries than WHAT you eat⁴⁷⁾.

However, more and more data in the literature show that the correlation between the intake frequency of fermentable carbohydrates and caries prevalence today is relatively weak in industrialised countries⁴⁸⁾. The most reasonable explanation for this is the widespread use of fluoride, especially in toothpaste, which increases the resistance to dental caries^49),50).

2.  Product-related dietary factors (=WHAT you eat)

The type and amount of carbohydrates are important. In addition to sucrose-containing food, PSSPs are being used increasingly frequently in many countries. Fructose, glucose and fructose corn syrup are also used in many commercial products today. The concentration of sugar and other fermentable carbohydrates is also essential for developing dental caries, even if there is no linear relationship between them.

Stickiness and chewing resistance (i.e. the physical and organoleptic properties of food) also influence its cariogenic potential. These two factors affect the eating pattern, the salivary secretion rate and the retention time (oral clearance) of food particles in the mouth. The oral sugar clearance of many foodstuffs has been studied extensively^51),52). High chewing resistance and fat in the food appear to speed up clearance from the mouth. There are also foods which lower the risk of caries^{53),54),55),3)}. As a result, different foodstuffs can have another cariogenic potential when evaluating WHAT you eat in relation to dental caries. This must be taken into consideration when relating diet to dental caries.

3.  Individual-related dietary factors (=HOW you eat)

In addition to the various product-related factors, at least three individual-related dietary factors are significant for dental caries: 1) the intake frequency, 2) the individual oral clearance and 3) the variation from one occasion to another (i.e. how often, how and when an individual eats) (Table 1)⁴⁷⁾. Numerous investigations have demonstrated that the number of meals or snacks a day appears to be the most critical factor for dental caries in overall terms^37),56),57). Regarding intake timing associated with the third factor, it is important to note that snacking before bedtime has been shown to pose a high potential risk of dental caries⁵⁸⁾. Prolonged periods between eating occasions can also lead to longer periods of time where the teeth are exposed to cariogenic food. For patient education, the sugar/PSSP clock model can be used to record a patient's starch intake frequency. The sugar clock, developed by Tandvärnet, a Swedish dental organisation, shows how frequently patients consume fermentable carbohydrates, including starch (Figure 5)⁵⁹⁾. Patients can be helped to understand that continuous acid attacks increase caries risk and that a reduced frequency helps maintain a healthy oral environment. Generally, consuming fermentable carbohydrates, including starchy staples, up to five times a day is safe, as there is sufficient time for remineralisation after each acid attack⁶⁰⁾.

Figure 5.

The sugar clock models for patient education on cariogenic food intake frequency^59）.　The sugar clock model, originally developed by Tandvärnet, serves as a tool for patient education regarding cariogenic food intake frequency. The upper model indicates a high-risk dietary pattern, while the lower model presents a low-risk dietary pattern.　Småätande - upprepat sockerintag = Stor risk för hål: Snacking - repeated sugar intake = High risk of cavities. LUNCH: LUNCH. MELLANMÅL: SNACK. MIDDAG: DINNER. FRUKOST: BREAKFAST. Regelbundna måltider - få sockerintag = Liten risk för hål: Regular meals - low sugar intake = Little risk of cavities.

Another dietary factor of importance for dental caries is individual oral clearance, expressed as the time it takes to eliminate the food from the mouth. Lanke (1957)⁵²⁾ and Hase et al. (1987)⁶¹⁾ showed that individuals differed widely in their ability to clear sugar- and starch-containing food from the oral cavity. Both these factors (frequency and oral clearance: i.e. how often and how an individual eats) are comparatively difficult to assess.

VI.  Japanese context

1.  Japanese food habits in different age groups

Compared with western countries, snack consumption is not a significant part of the Japanese diet, but it is gradually becoming more westernised, with the increasing consumption of bread, dairy, animal food and oil^62),63). In Japan, young children aged three to six years had a higher percentage (19.5%) of snack energy intake of total energy intake than adults aged 20 to 69 years (11%)^64),63). Additionally, while older Japanese people tended to follow traditional Japanese dietary patterns (i.e. Washoku), younger generations exhibited the characteristics of a more westernised diet⁶⁵⁾. Some Japanese people exhibited unhealthy eating behaviour, such as snacking, eating quickly, eating late evening meals and skipping breakfast, and the accumulation of these habits was associated with overweight and obesity in Japanese populations^66),67).

2.  Marketing of PSSPs

The marketing of PSSPs has become widespread and diverse in recent years¹⁾. PSSPs are often promoted as convenient, tasty and quick energy sources. However, it is essential to acknowledge that these products are not necessarily healthy, especially for oral health. One of the strategies used by manufacturers to make PSSPs more appealing, which is often seen in Japan, is to add healthy ingredients such as calcium, vitamins, citric acid or potassium, or to bake or fry these products with vegetable oils⁶⁸⁾. These products are advertised as nutritious, healthy and low in fat, leading people to believe they will become healthier. However, the reality is that adding calcium or vitamins or using vegetable oils does not reduce the cariogenicity of products. Some of these products may be more cariogenic than those without added ingredients. For example, adding flavours and sweeteners to PSSPs may increase the acidity of the oral environment, promoting demineralisation and erosion.

Furthermore, flavoured or sweetened starch snacks may lead to overconsumption, contributing to not only dental caries but also other overweight-related diseases²⁾. The United Nations, the World Health Organisation and the United Nations International Children's Emergency Fund have urged restricting the marketing of unhealthy food, including PSSPs, to children⁶⁹⁾. The marketing of unhealthy food to vulnerable children is ethically questionable and raises concerns about prioritising profits over the well-being of individuals⁷⁰⁾.

3.  How to interpret scientific evidence in the Japanese context

There are varying opinions among Japanese dental professionals regarding the connection between starch and dental caries, owing to the complexity of the issue. The cariogenicity of starch should not be denied^71),72), as it also possesses the potential to induce periodontal diseases⁷³⁾. However, the term “starch” alone does not sufficiently address the debate⁹⁾. It is essential to clarify “WHAT and HOW an individual eats” before discussing the cariogenicity of starch, as mentioned previously.

Some researchers may propose that Japanese dietary habits differ from those in western countries and the potential cariogenicity of PSSPs may not be as significant in Japan as it is in the west, where a consensus report by cariologists and periodontologists recommended promoting the absence of processed foods for preschool and school children for caries prevention to dental teams and policymakers⁷³⁾. In fact, the mean daily snack frequency in Japan was within the safe threshold⁶³⁾. Compared with the west, the proportion of daily energy intake consumed from snacks was lower in Japan^64),63). Frequently snacking on cookies, Japanese crackers or bread did not increase the risk of early childhood caries among 18- to 23-month-old Japanese toddlers in a cross-sectional study⁵⁸⁾.

However, it is worth noting that, in the study by Murakami et al. (2022)⁶³⁾, the frequency of daily snacks varied widely among individuals, ranging from zero to eight snacks a day. Dental caries is a complex condition influenced by multiple factors, including fluoride use, dietary habits, microbiota composition, saliva, oral hygiene practices and genetics, for example, all of which vary in strength from person to person. Furthermore, among Japanese studies, the heterogeneity of fluoride effect for caries prevention has been seen⁵⁸⁾, although it has been admitted that the fluoride factor has the strongest impact on caries prevention⁷⁴⁾. The unique context of fluoride use in Japan may include factors such as the weak fluoride concentration traditionally recommended, an inadequate amount of fluoride toothpaste used and the thorough rinsing of fluoride toothpaste, which may make Japanese research results not directly comparable to international findings.

As a result, to enhance public health, it is crucial to examine the results critically, standardise each term and condition in accordance with international norms and thoroughly investigate and discuss the underlying reasons behind the research and survey findings. In clinics, personalised advice and regular dental check-ups with a comprehensive assessment are essential to control the risk of caries in order to prevent dental caries. Additionally, dental hygienists should educate patients on the associations between PSSPs and overweight-related diseases including dental caries from a holistic perspective^75),31),35).

VII.  Conclusion and clinical relevance

Starch is a type of fermentable carbohydrate that is hydrolysed in the oral cavity into cariogenic sugars. The cariogenic potential of starch food products is complex; the order of cariogenicity is from the lowest to the highest: raw starch, processed starch, sucrose alone, or a starch-sucrose combination. PSSPs have three aspects that contribute to their cariogenicity: bioavailability, retentive properties and consumption frequency. Those individuals with dry mouth, who snack on these products with a starch-sucrose combination, run a comparatively high risk of caries. When evaluating the diet from a cariological perspective, two dietary factors: product and individual related, need to be considered and HOW frequently you eat is more important for caries than WHAT you eat. Recent changes in Japanese food habits, with an increasing preference for PSSPs and a prevalence of unhealthy eating behaviours, have raised concerns about the potential adverse health impacts. Personalised advice and check-ups based on risk assessment should be conducted for caries prevention, along with a holistic perspective.

Acknowledgements

We would like to express our sincere gratitude to Ms Jeanette Kliger for her valuable contributions in editing and refining the English language in this paper. We also thank Mr Jesse Cordova for generously dedicating his time to review the proofs.JSPS KAKENHI Grant Number JP22K13751 provided the financial assistance for this study.

The authors declare no conflict of interest.

Supplement 1:

The search strategy

Supplement 2:

The predetermined inclusion criteria

Supplement 3:

The flow chart showing the numbers of included and excluded articles

Supplement 4:

The list of excluded articles and the main reason for exclusion

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