prevalence of black stain and associated risk factors in preschool spanish children

5
Original Article Prevalence of black stain and associated risk factors in preschool Spanish children Jose Manuel Garcia Martin, 1 Manuel Gonzalez Garcia, 1 Juan Seoane Leston, 2 Santiago Llorente Pendas, 1 Juan Jose Diaz Martin 1 and Maria Jose Garcia-Pola 1 1 School of Medicine, Oviedo University, Oviedo and 2 Faculty of Dentistry, USC, Santiago de Compostela, Spain Abstract Background: In pediatric clinical practice, it is common to be asked about the presence of black stains on teeth in children and teenagers. According to controversial etiology, it is known to be related to a low rate of caries. The aim of this study was to determine the prevalence of black stain and associated risk factors in Spanish preschool children. Methods: A total of 3272 children aged 6 years old (3058 non-emigrant and 214 immigrant children) living in Oviedo (Spain), were enrolled in the present study. Results: The prevalence of black stain was 3.1% in the whole group. The index of primary decayed, missing, and filled teeth (dmft index) associated with black stain was 0.35 1.123. A statistical association between black stain and the consumption of iron supplements was noted. Conclusions: The regular consumption of foods rich in iron and the use of iron supplements during pregnancy and early childhood, could favor the development of chromogenic microbiota. The prevalence of black stain did not differ significantly between non-emigrant and immigrant children in Spain. Key words black stain, chromogenic bacteria, dental caries, iron supplements, preschool children. In pediatric clinical practice, it is common to be asked about the presence of black stains on teeth in children and teenagers. This is called black stain and, according to Reid et al., it has been defined as: pigmented dark lines parallel to the gingival margin or an incomplete coalescence of dark dots rarely extend- ing beyond the cervical third of the crown. 1 Its formation is attributed to the colonization of the membrane of Nasmyth by chromogenic bacteria belonging to the following families: Porphyromonas, Prevotella and Actinomyces, which require vitamin K and hemin for development. 2,3 Traditionally, the presence of secondary black stain is related to the presence of chromogenic bacteria, with a low rate of dental caries. 4,5 The reported prevalence of black stain varies from study to study, according to subject age and country of origin. In Europe, it ranges from 1.6% (UK), 6 4.45% (Poland), 7 6.3% (Italy), 4 to 7.54% (Valencia, Spain). 8 In South America, it ranges from 6.5% (Peru) 9 to 14.8% (Brazil). 10 On the Asian continent, it varies from 16% (Philippines) 11 to 18% (India). 12 According to the International Organization for Migration, a substantial amount of immigrants have joined the Spanish native population. Thus, in the last census conducted in 2010, it was estimated that they exceeded 14% of the total number of inhabitants. 13 So far, no study has been carried out on the prevalence of black stain in a large group of subjects of the same age, which would integrate different races and habits and which would permit identification of the contributions of the various habits and lifestyles to the production of black stain. The purpose of this paper was therefore to evaluate the preva- lence of black stain on teeth in two groups of 6-year-old children: one of Spanish origin and the other of emigrant origin, as well as the influence of certain sanitary determinants, eating habits and oral hygiene. Methods The study includes 3272 6-year-old children, 3058 native chil- dren (G1) and 214 immigrant children (G2) who had dental check-up at the Vallobin Heath Centre – La Florida, in Oviedo (Spain), between January 1998 and March 2011. The dental check-up was performed in a dental office and performed by only one dentist. A record was prepared with the following data: sex, country of origin, presence of black stain, index of primary decayed, missing, and filled teeth (dmft index), oral simplified debris index, number of previous visits to the dentist, duration of ges- tation, mode of delivery at birth, birthweight, type of feeding (breast milk; formula; mixed), record of iron supplement con- sumption during gestation and childhood, and survey of eating habits and oral hygiene, including consumption of meat, fish, vegetables, legumes, fresh fruits, dairy products, bread, pasta and rice, eggs, type of soft drinks with or without sugar, natural Correspondence: Maria Jose Garcia-Pola Vallejo, PhD, School of Medicine, Oviedo University, c/ Julian Clavería s/n. 33006 Oviedo, Spain. Email: [email protected] Received 2 May 2012; revised 13 January 2013; accepted 1 February 2013. Pediatrics International (2013) 55, 355–359 doi: 10.1111/ped.12066 © 2013 The Authors Pediatrics International © 2013 Japan Pediatric Society

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Page 1: Prevalence of black stain and associated risk factors in preschool Spanish children

Original Article

Prevalence of black stain and associated risk factors in preschoolSpanish children

Jose Manuel Garcia Martin,1 Manuel Gonzalez Garcia,1 Juan Seoane Leston,2 Santiago Llorente Pendas,1

Juan Jose Diaz Martin1 and Maria Jose Garcia-Pola1

1School of Medicine, Oviedo University, Oviedo and 2Faculty of Dentistry, USC, Santiago de Compostela, Spain

Abstract Background: In pediatric clinical practice, it is common to be asked about the presence of black stains on teeth inchildren and teenagers. According to controversial etiology, it is known to be related to a low rate of caries. The aim ofthis study was to determine the prevalence of black stain and associated risk factors in Spanish preschool children.Methods: A total of 3272 children aged 6 years old (3058 non-emigrant and 214 immigrant children) living in Oviedo(Spain), were enrolled in the present study.Results: The prevalence of black stain was 3.1% in the whole group. The index of primary decayed, missing, and filledteeth (dmft index) associated with black stain was 0.35 � 1.123. A statistical association between black stain and theconsumption of iron supplements was noted.Conclusions: The regular consumption of foods rich in iron and the use of iron supplements during pregnancy and earlychildhood, could favor the development of chromogenic microbiota. The prevalence of black stain did not differsignificantly between non-emigrant and immigrant children in Spain.

Key words black stain, chromogenic bacteria, dental caries, iron supplements, preschool children.

In pediatric clinical practice, it is common to be asked about thepresence of black stains on teeth in children and teenagers.

This is called black stain and, according to Reid et al., it hasbeen defined as: pigmented dark lines parallel to the gingivalmargin or an incomplete coalescence of dark dots rarely extend-ing beyond the cervical third of the crown.1

Its formation is attributed to the colonization of the membraneof Nasmyth by chromogenic bacteria belonging to the followingfamilies: Porphyromonas, Prevotella and Actinomyces, whichrequire vitamin K and hemin for development.2,3

Traditionally, the presence of secondary black stain is relatedto the presence of chromogenic bacteria, with a low rate of dentalcaries.4,5

The reported prevalence of black stain varies from study tostudy, according to subject age and country of origin.

In Europe, it ranges from 1.6% (UK),6 4.45% (Poland),7 6.3%(Italy),4 to 7.54% (Valencia, Spain).8 In South America, it rangesfrom 6.5% (Peru)9 to 14.8% (Brazil).10 On the Asian continent, itvaries from 16% (Philippines)11 to 18% (India).12

According to the International Organization for Migration,a substantial amount of immigrants have joined the Spanishnative population. Thus, in the last census conducted in 2010, itwas estimated that they exceeded 14% of the total number ofinhabitants.13

So far, no study has been carried out on the prevalence ofblack stain in a large group of subjects of the same age, whichwould integrate different races and habits and which wouldpermit identification of the contributions of the various habits andlifestyles to the production of black stain.

The purpose of this paper was therefore to evaluate the preva-lence of black stain on teeth in two groups of 6-year-old children:one of Spanish origin and the other of emigrant origin, as well asthe influence of certain sanitary determinants, eating habits andoral hygiene.

Methods

The study includes 3272 6-year-old children, 3058 native chil-dren (G1) and 214 immigrant children (G2) who had dentalcheck-up at the Vallobin Heath Centre – La Florida, in Oviedo(Spain), between January 1998 and March 2011.

The dental check-up was performed in a dental office andperformed by only one dentist.

A record was prepared with the following data: sex, countryof origin, presence of black stain, index of primary decayed,missing, and filled teeth (dmft index), oral simplified debrisindex, number of previous visits to the dentist, duration of ges-tation, mode of delivery at birth, birthweight, type of feeding(breast milk; formula; mixed), record of iron supplement con-sumption during gestation and childhood, and survey of eatinghabits and oral hygiene, including consumption of meat, fish,vegetables, legumes, fresh fruits, dairy products, bread, pasta andrice, eggs, type of soft drinks with or without sugar, natural

Correspondence: Maria Jose Garcia-Pola Vallejo, PhD, School ofMedicine, Oviedo University, c/ Julian Clavería s/n. 33006 Oviedo,Spain. Email: [email protected]

Received 2 May 2012; revised 13 January 2013; accepted 1February 2013.

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Pediatrics International (2013) 55, 355–359 doi: 10.1111/ped.12066

© 2013 The AuthorsPediatrics International © 2013 Japan Pediatric Society

Page 2: Prevalence of black stain and associated risk factors in preschool Spanish children

juices, artificial juices, and the use of toothpaste with fluoride,without fluoride, mouthwash with or without fluoride.

Children born outside Spain, but who had lived �3 years inSpain, were not included in the study.

We used the criterion proposed by Theilade et al. to detect thepresence of black stain.14 The WHO criteria were used to calcu-late the dmft index15 and the simplified debris index of Green andVermillion.16

The frequency of consumption of specified food was classi-fied into three categories: �3 times/month, �6 times/week and�1 times/day. As for the oral hygiene habits: brushing teeth withtoothpaste with or without fluoride and mouthwash with orwithout fluoride �6 times/week, 1 time/day and �2 times/day.

The consumption of iron supplements in the previous 6months was not recorded.

The children’s caregivers were given a document with infor-mation, and informed consent to be included in the study as wellas the survey of eating habits and oral hygiene.

Data were collected in a database created ad hoc for the studyand analyzed on a PC with SPSS (Statistical Productor ServiceSolutions) version 18.0 (University of Oviedo). Data are given asmean � SD and 95% confidence interval. Comparisons betweenmeans were performed using Student’s unpaired t-test. Chi-squared test was used to analyze qualitative variables. Two-tailedP < 0.05 was deemed statistically significant.

Results

The sample consisted of 3272 children: 1721 boys and 1551 girls.The ratio of boys to girls in each group was 1.1 in G1 and 0.94in G2.

The prevalence of black stain was 3.1% in the total sample(G1, 3.1%; G2, 1.9%). The prevalence of black stain did notdiffer significantly between the two groups (P = 0.416), nor wasthere any statistically significant association between sex andblack stain.

The dmft index for the whole group was 0.64 � 1.834. Thedmft index associated with black stain was 0.35 � 1.123 in thewhole group, 0.36 � 1.144 in G1 and 0 in G2. The associationbetween black stain and dmft index was not deemed statisticallysignificant in the whole group (P = 0.969), nor in G1 (P = 0.977)or G2 (P = 1; Table 1).

For 74.3% of the children in the whole group and 76% of thechildren with black stain, this was the first time they had come toa dental check-up performed by a dentist.

No statistically significant relationship were found betweensimplified debris index, mode of delivery, type of feeding (breastmilk; formula; mixed), black stain and dmft index.

Ten per cent of the children with black stain had been low-birthweight premature babies.

A statistically significant association was seen in the wholegroup with regard to premature delivery (P = 0.05) and lowbirthweight (P = 0.007), and in G1 for premature delivery (P =0.003) and low birthweight (P = 0.003).

A total of 11% of the children with black stain had consumediron supplements, while 2.7% of the children without black stainconsumed iron supplements. Ta

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356 JM Garcia Martin et al.

© 2013 The AuthorsPediatrics International © 2013 Japan Pediatric Society

Page 3: Prevalence of black stain and associated risk factors in preschool Spanish children

There was a statistically significant association between thepresence of black stain and consumption of iron supplements inthe whole group (P = 0.000), and in G1 (P = 0.000) and G2 (P =0.030). There was also a statistically significant associationbetween the previous use of iron supplements by the motherduring pregnancy and the detection of black stain, in the wholegroup (P = 0.006) and in G1 (P = 0.003).

There was a statistically significant association between thedetection of black stain and the consumption of certain types offood, and oral hygiene habits (Table 2).

Discussion

The prevalence of black stain in this study was 3.1%. This ishigher than in the UK (1.6%),6 and lower than Poland (4.45%),7

Italy (6.3%),4 Valencia (7.54%),8 the Philippines (16%),11 andIndia (18%),12; this may be due to the difference in age of thecohorts.

In the present study, 74.3% of the G2 children (214 children),came from South American countries. The present G2 childrenhad a 1.9% prevalence of black stain, which contrasts with thedata previously observed for some countries of South America.

Gasparetto et al. observed black stain in 14.8% of 263 Bra-zilian children aged between 6 and 12 years old.10

Another study carried out in Peru reported a prevalence of6.5% in the mixed dentition of 185 children.9

In the present study, both the prevalence of black stainobserved in the whole group (3.1%) and in the G1 (native) chil-dren, are the lowest observed and are closer to those obtained inEuropean countries. In contrast, the prevalence observed in G2(1.9%), consisting of emigrant children, differs from the highvalues observed in the non-European countries.

These differences could be justified, not just by the qualitativecharacteristics (racial origin and age of the group studied), butalso by the quantitative characteristics, such as the size of thegroup.

Thus, if we compare the data on group size and homogeneityof the age of the group, we find only five studies in which thesubject group is larger than 1000 children.4,7,8,11,12 The presentstudy has the largest group (3272 children), followed by a studyof Polish children with a sample size of 3125,7 which almostduplicates the next most numerous group studied with 1748Filipino children.11

As for the age of the children studied, there is no uniformity,and it ranges between 4 and 12 years old. To date, there has beenno study carried out on a homogeneous age group.

The dmft index found in the present group was 0.64 � 1.834,which is close to that observed in a study carried out nationwidein 2007 in Spain in preschool children aged 4 years old, in whichthe dmft index obtained was 0.76, and in which immigrant chil-dren were also included.17

As for the association between the presence of black stain andcaries in the current study, we observed that the children withblack stain had a dmft index of 0.35 � 1.123, lower than thatobserved in children without black stain, whose dmft index was0.65 � 1.852. Ta

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Black stain prevalence and risk factors 357

© 2013 The AuthorsPediatrics International © 2013 Japan Pediatric Society

Page 4: Prevalence of black stain and associated risk factors in preschool Spanish children

Most authors report the association of the presence of blackstain with a low index of caries. Thus, Sutcliffe noted that inchildren who had black stain the DMFT index was 3.06 � 0.50,and for those without black stain the DMFT index was 5.67 �

0.13.6 Paredes and Paredes found that 32.5% of the children intheir group had caries, and that among those, only 6.9% hadblack stain.8 Koch et al. found a DMFT index of 1.87 � 2.47associated with black stain, and a DMFT index of 2.39 � 2.62 forlack of black stain.4 In Peru, Mayta-Tovalino and Torres-Quevedoobserved a DMFT index of 1.33 � 1.073 associated with blackstain, and a DMFT index of 3.39 � 2.391 for lack of black stain.9

Gasparetto et al. observed that only 28.1% of his group did nothave any caries, and among the group without caries, 84% wereassociated with black stain.10 Heinrich-Weltzien et al. observed aDMFT index associated with black stain of 1.5 � 2.1, and aDMFT index of 2.5 � 2.5 for lack of black stain.11 In India, Bhatfound a DMFT index of 1.12 � 1.41 associated with black stain,and a DMFT index of 1.77 � 1.87 for lack of black stain.12

Given the results of the other studies listed here, even thougha statistically significant association was not obtained in thepresent study, the present observed trend of a low index of cariesassociated with black stain, is corroborated by the other studies.

And even though there was no statistically significant rela-tionship between level of oral hygiene and the presence of blackstain, it is worth noting that 74.3% of the group had not previ-ously had a dental check-up, and the percentage of children withblack stain who had come for the first time was 76%.

These data contrast with the recommendations of the maindental associations, which advise having the first dental check-upperformed by a dental health professional during the first year.18

On the basis of the present results, however, the dental health ofthree out of four of the present children had been examined byprofessional pediatricians. Professional pediatricians periodi-cally examine most of the children during the early years and arefrequently asked by their parents about the dental problems oftheir children.19,20

In the present study we did not find any statistically significantrelationship between the level of oral hygiene and black stain inthe whole group, neither in G1 nor in G2 (P = 0.478). This agreeswith the findings in the Sutcliffe and in the Mayta-Tovalino andTorres-Quevedo studies.6,9

There was a statistically significant relationship, however,between the presence of black stain and the consumption of ironsupplementation during pregnancy (P = 0.006), and in child-hood (P = 0.000). In the Mayta-Tovalino and Torres-Quevedostudy a similarly statistically significant relationship was found(P = 0.027).9

Even though there was no statistically significant associationbetween the consumption of iron supplementation and dmftindex, we detected caries in only one of the children with blackstain and who had taken iron supplementation.

In experimental studies carried out on animals, it wasobserved that a diet that includes iron supplements reduces theacidogenic capacity of the dental plaque21 and is associated witha lower number of caries.22 Shaoul et al. have observed severedental caries in children with iron deficiency.23

As for the interpretation of the data on eating habits, thepresent study may have some limitations due to information andinterpretation biases, with regard to the information the chil-dren’s parents were asked about, as well as the bias in recall ofthis information.

We emphasize the present finding of a statistically significantrelationship between black stain and the consumption offood with a high iron content as well as beverages containingvitamin C.

Just as there are foods that can have cariostatic effects, exert-ing a modulating effect on the cariogenic bacteria and the com-position of the saliva,24 the consumption of specific foods rich iniron, such as vegetables, legumes, dairy products and eggs islikely to favor the growth and colonization of the oral cavity bythe involved bacteria in the development of black stain. Thus, intheir studies, Surdacka, and Reid and Beeley found in the com-position of the saliva of the children who had black stain asignificant increase of various microelements such as calciumand phosphates. Moreover, they observed that the chemical com-position of the saliva in children and teenagers with black stainwas associated with a low susceptibility to dental caries, consid-ering that the high levels of phosphate could contribute toincrease the buffering capacity of the saliva acidity against thedental plaque.25,26

The interplay between black stain, caries, oral microflora anddiet remains unclear and requires further research.

In the survey on hygiene habits, we found a statistically sig-nificant relationship between the presence of black stain and thefollowing hygiene habits: teeth brushing with fluoride toothpasteand with fluoride rinse.

An adequate supply of fluoride, above all while using tooth-paste and fluoride mouthwashes, provides both the saliva and theplaque with an abundance of that ion, which can reduce theacidogenic capacity of the dental plaque,27 which in turn canfavor the development of another type of microbiota, as well asthe chromogenic.

Conclusions

Regular consumption of foods rich in iron and use of iron sup-plements during pregnancy and early childhood could favor thedevelopment of chromogenic microbiota.

The prevalence of black stain did not differ significantlybetween non-emigrant and immigrant children in Spain.

References

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2 Watts A, Addy M. Tooth discoloration and staining: A review of theliterature. Br. Dent. J. 2001; 190: 309–16.

3 Saba C, Solidani M, Berlutti F, Vestri A, Ottolenghi L, Polimeni A.Black stains in the mixed dentition: A PCR microbiological studyto the etiopathogenic bacteria. J. Clin. Pediatr. Dent. 2006; 30:219–24.

4 Koch MJ, Bove M, Schroff J, Perlea P, Garcia-Godoy F, StaehleHJ. Black stain and dental caries in schoolchildren in Potenza,Italy. ASDC J. Dent. Child. 2001; 68: 353–5.

5 Slots J. The microflora of black stain of human primary teeth. Scan.J. Dent. Res. 1974; 82: 484–90.

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6 Sutcliffe P. Extrinsic tooth stains in children. Dent. Pract. Dent.Rec. 1967; 17: 175–9.

7 Surdacka A. Black stain and caries in children and adolescents inschools. Czas. Stomatol. 1987; 40: 763–9.

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13 International Organization for Migration. IOM, World MigrationReport 2010. [Cited 12 January 2012.] Available from URL: http://www.publications.iom.int.

14 Theilade J, Slots J, Fejerskov O. The ultrastructure of black stainon human primary teeth. Scand. J. Dent. Res. 1973; 81: 528–32.

15 World Health Organization. Oral Health Surveys: Basic Methods,4th edn. World Health Organization, Geneva, 1997.

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17 Bravo M, Llodra JC, Cortes FC et al. Encuesta de Salud Oral dePreescolares en España 2007. RCOE 2006; 12: 143–68.

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Clinical Affairs. Policy on dietary recommendations for infants,children and adolescents. Pediatr. Dent. 2008–2009; 30 (7 Suppl.):47–8.

19 Bottenberg P, Van Melckebeke L, Louckx F, Vandenplas Y.Knowledge of Flemish paediatricians about children’s oral health:Results of a survey. Acta Paediatr. 2008; 97: 959–63.

20 Balaban R, Aguiar CM, Da Silva Araújo AC, Dias Filho EB.Knowledge of paediatricians regarding child oral health. Int. J.Paediatr. Dent. 2011; 17: 1–6.

21 Miguel JC, Bowen WH, Pearson SK. Effects of iron salts insucrose on dental caries and plaque in rats. Arch. Oral Biol. 1997;42: 337–83.

22 Emilson CG, Krasse B. The effect of iron salts on experimentaldental caries in the hamster. Arch. Oral Biol. 1972; 7: 1439–43.

23 Shaoul R, Gaitini L, Kharouba J, Darawshi G, Maor I, Somri M.The association of childhood iron deficiency anaemia with severedental caries. Acta Paediatr. 2012; 101: 76–9.

24 Moynihan P. Foods and dietary factors that prevent dental caries.Quintessence Int. 2007; 38: 320–24.

25 Surdacka A. Chemical composition of the saliva in childrenand adolescents with black tartar. Czas. Stomatol. 1989; 42: 525–33.

26 Reid JS, Beeley JA. Biochemical studies on the composition ofgingival debris from children with black extrinsic tooth stain.Caries Res. 1976; 10: 363–9.

27 World Health Organization. Fluorides and oral health. Re-port of a WHO Expert Committee on Oral Health Status andFluoride Use. World Health Organ. Tech. Rep. Ser. 1994; 846:1–37.

Black stain prevalence and risk factors 359

© 2013 The AuthorsPediatrics International © 2013 Japan Pediatric Society