This study compared dietary fluoride intake in children aged 4-6 years from communities receiving different sources of systemic fluoride: artificially fluoridated water in Brazil (0.6-0.8 mg/L), naturally fluoridated water in Brazil (0.6-0.9 mg/L), fluoridated salt in Peru (180-200 mg/kg), fluoridated milk in Peru (0.25 mg), and a non-fluoridated community. Dietary intake was measured using duplicate diets collected over two days. Mean fluoride intake was highest in communities receiving fluoridated water and lowest in the non-fluoridated community. The main dietary contributors of fluoride also differed between communities receiving water fluor

1. Journal of Dental Research
http://jdr.sagepub.com/
Dietary Fluoride Intake by Children Receiving Different Sources of Systemic Fluoride
M.H.C. Rodrigues, A.L. Leite, A. Arana, R.S. Villena, F.D.S. Forte, F.C. Sampaio and M.A.R. Buzalaf
J DENT RES 2009 88: 142
DOI: 10.1177/0022034508328426
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2. ReSeaRCH RePoRtS
Clinical
M.H.C. Rodrigues1, A.L. Leite1,
A. Arana2, R.S. Villena2, F.D.S. Forte3, Dietary Fluoride Intake by
F.C. Sampaio3, and M.A.R. Buzalaf1* Children Receiving Different
1
Department of Biological Sciences, Bauru Dental School, Sources of Systemic Fluoride
University of São Paulo, Al. Octávio Pinheiro Brisolla, 9-75,
Bauru, SP, 17012-901, Brazil; 2Peruvian University Cayetano
Heredia, Lima, Peru; and 3Health Science Center, Federal
University of Paraíba, João Pessoa, PB, Brazil; *correspond-
ing author, mbuzalaf@fob.usp.br
J Dent Res 88(2):142-145, 2009
INTRODUCTION
T
abStRaCt he prevalence and severity of dental caries in most industrialized coun-
There has been no comparison of fluoride (F) tries have decreased dramatically over the last decades (Marthaler,
intake by pre-school children receiving more tradi- 2004; Burt and Eklund, 2005). One of the main reasons for the caries
tional sources of systemic F. The aim of this study prevalence decline is the widespread use of fluoride (F), including water
was to estimate the dietary F intake by children fluoridation (Bratthall et al., 1996).
receiving F from artificially fluoridated water Water fluoridation reaches an entire population, including socially under-
(AFW-Brazil, 0.6-0.8 mg F/L), naturally fluori- served groups with the highest levels of caries, and systematic reviews have
dated water (NFW-Brazil, 0.6-0.9 mg F/L), fluori- acknowledged its benefits (McDonagh et al., 2000; National Health and
dated salt (FS-Peru, 180-200 mg F/Kg), and Medical Research Council, 2007). It has been shown that this method reduces
fluoridated milk (FM-Peru, 0.25 mg F). Children the DMFT by, on average, 2.25 teeth per child and increases the proportion
(n = 21-26) aged 4-6 yrs old participated in each of caries-free children by 15%. Moreover, there appears to be some evidence
community. A non-fluoridated community (NoF) that it reduces the inequalities in dental caries across social classes in 5- and
was evaluated as the control population. Dietary F 12-year-olds (McDonagh et al., 2000). However, for political, geographical,
intake was monitored by the “duplicate plate” and technical reasons, the benefits of water fluoridation are unavailable to a
method, with different constituents (water, other large proportion of the world’s population (Armfield, 2007). Therefore, other
beverages, and solids). F was analyzed with an ion- methods of community fluoridation have been suggested—for example, salt,
selective electrode. Data were tested by Kruskall- sugar, and milk (Horowitz, 1990; Kumar and Moss, 2008).
Wallis and Dunn’s tests (p < 0.05). Mean (± SD) F Simultaneous with the caries decline, an increase in the prevalence of
intake (mg/Kg b.w./day) was 0.04 ± 0.01b, 0.06 ± dental fluorosis has been observed in many countries (Khan et al., 2005).
0.02a,b, 0.05 ± 0.02a,b, 0.06 ± 0.01a, and 0.01 ± 0.00c This implies that the sources of F intake by children at risk for dental
for AFW/NFW/FS/FM/NoF, respectively. The main fluorosis warrant investigation. Additionally, the literature correlating F
dietary contributors for AFW/NFW and FS/FM/ intake and dental fluorosis is scarce (Martins et al., 2008), and the “opti-
NoF were water and solids, respectively. The results mum” daily F intake to avoid dental fluorosis has been empirically estab-
indicate that the dietary F intake must be consid- lished (Burt, 1992; Guha-Chowdhury et al., 1996). In Latin American
ered before a systemic method of fluoridation is countries where different national fluoridation methods have been imple-
implemented. mented for decades, only a few data on F intake are available (Paiva et al.,
2003; Levy et al., 2004; Franco et al., 2005; Pessan et al., 2005; Almeida
et al., 2007). Few surveys have been performed (for review, see Buzalaf and
Kobayashi, 2007), but there is no comparison of F intake by preschool
Key woRDS: exposure, fluoride, diet, children, children with different sources of systemic F. The aim of this study was to
fluorosis. estimate dietary F intake by children receiving systemic F from different
sources, considering the different constituents of the diet (drinking water,
other beverages, and solids).
MATERIALS & METHODS
Participants
Ethical approval was obtained from the Institutional Review Boards (IRB) of
Bauru Dental School (no. 116/2004) and Peruvian University Cayetano
Heredia, as well as from the Brazilian National Research Council (no. 11174).
DOI: 10.1177/0022034508328426 Parents signed an IRB-approved consent document.
Received January 16, 2008; Last revision September 11, 2008; The participants in this multicentric study were 4- to 6-year-old children
Accepted October 15, 2008 receiving systemic F from different sources: artificially fluoridated water
142
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3. J Dent Res 88(2) 2009 F Intake by Preschool Children 143
(Bauru, Brazil, 316,000 inhabitants, Human Development Index- 0.095, 0.190, 0.950, 1.900, and 4.750 µg F) were prepared by
HDI 0.825, 0.6-0.8 mg F/L, n = 25), naturally fluoridated water serial dilution of a stock standard containing 0.1 M F (Orion
(Brejo dos Santos, Brazil, 6000 inhabitants, HDI 0.613, 0.6-0.9 940906) in triplicate and diffused as the samples. In addition,
mg F/L, n = 21), fluoridated salt (Lima, Peru, 8,400,000 inhabit- non-diffused F standards were prepared with the same solution
ants, HDI 0.767, 180-200 mg F/Kg, n = 26), and fluoridated milk (0.05 M NaOH, 0.20 M acetic acid, plus NaF) for preparation of
(Trujillo, Peru, 747,000 inhabitants, HDI 0.673, 250 mL of milk the diffused standards and samples. The non-diffused standards
containing 1.0 mg F/L, n = 25). The fluoridation schemes were had exactly the same F concentration as the diffused standards.
implemented in 1975, 1986, and 1999 in Bauru, Lima, and Comparison of the millivolt readings demonstrated that F in the
Trujillo, respectively. A non-fluoridated community (Pirajuí, diffused standards was completely trapped and analyzed (recov-
Brazil, 20,000 inhabitants, HDI 0.779, n = 24) was included as a ery > 99%). The millivoltage potentials were converted to µg F
negative control population. All children enrolled were lifelong by a standard curve (r ≥ 0.99). All samples were analyzed in
residents of their respective communities and drank water from duplicate. The mean repeatability of the readings, based on
the public supply only. They had good oral health, were not using duplicate samples, was 96.7% for solids and 96.8% for other
medicines or topical fluorides, and had no gastrointestinal, bone, beverages.
or health problems. Children who participated were not chosen F analyses in the water samples were performed by means of
randomly, since parental permission had been granted, and the an ion-specific electrode (Orion 9609), after sample buffering
source of systemic F intake had been previously checked. Sample with an equal volume of TISAB II. Standards (containing 0.1,
size was calculated based on a previous study (Levy et al., 2004), 0.2, 0.4, 0.8, 1.6, and 3.2 mgF/L) were prepared by serial dilu-
to ensure a and b errors of 5% when fluoridated and non-fluori- tion of 100 mgF/L NaF stock solution (Orion). The standard
dated communities were compared. curves had a correlation coefficient ≥ 0.99. All samples were
analyzed in duplicate. The mean repeatability of the readings,
based on duplicate samples, was 98.5%.
Collection of Duplicate Diets
The daily dietary F intake of the children was estimated by the Statistical analysis
“duplicate plate” method, as described previously (Almeida et
al., 2007), with a slight modification that consisted of collect- The software GraphPad Prism 4 version 4.0 for Windows
ing water samples separately from milk samples, which were (GraphPad, San Diego, CA, USA) was used. The assumptions of
collected together with other beverages in the diet, since equality of variance and normal distribution of errors were
Trujillo has fluoridated milk. Thus, the constituents of the diet checked for all the variables tested. Since the distribution of the
were collected separately (solids, water, and other beverages) errors was not homogeneous, data were tested by Kruskall-Wallis
in plastic vials (1000 mL), on two consecutive days, simulta- and Dunn’s tests for individual comparisons among the groups.
neously in all communities. Parents were instructed to main- A statistical significance level of 5% was selected a priori.
tain the usual dietary habits of their children and to duplicate
the diet as precisely as possible (for details, see Guha-
Chowdhury et al., 1996). Diets were immediately homoge-
RESULTS
nized with a known volume of de-ionized water. The total Data are expressed as mean (± SD). Mean F concentrations in
volume (or total weight for solids) was measured, and a 50-mL tap water collected at the children’s houses were 0.70 ± 0.08,
aliquot was taken and frozen (-20ºC). Samples were kept fro- 0.66 ± 0.20, 0.04 ± 0.05, 0.49 ± 0.03, and 0.08 ± 0.01 mg/L for
zen while shipped to the analytical laboratory. Children were Bauru (Brazil, artificially fluoridated water), Brejo (Brazil,
weighed (± 0.1 Kg) on calibrated electronic scales (model naturally fluoridated water), Lima (Peru, fluoridated salt),
HS301, Tanita Corporation, Arlington Heights, IL, USA). Trujillo (Peru, fluoridated milk), and Pirajuí (Brazil, non-
Their weights were recorded for calculation of the F intake fluoridated), respectively.
(mg/Kg body weight). The Table shows the F intake from dietary components (sol-
ids, water, and other beverages) and total diet. There was a
significant difference among the communities regarding the
tap water Collections
F intake from solids (KW = 87.49, p < 0.0001), and in Lima and
Since fluctuations in public water F levels have been described in Trujillo, the data were not significantly different, but were
Bauru (Buzalaf et al., 2002a), two samples of tap water were col- higher when compared with data from the other communities
lected at the children’s houses on the same day as diet collection. (p < 0.01). Despite the fact that Bauru had higher amounts of
Water samples were frozen (-20ºC) until F analysis. F intake from solids when compared with Brejo, this difference
was not statistically significant. All the communities except
Brejo had amounts of F intake from solids significantly higher
analytical Procedure
than those from Pirajuí, the control community (p < 0.01).
F concentrations in the diet (solids and other beverages, separately) The mean volume of water ingested per day during the two
samples were determined after overnight hexamethyldisiloxane days of duplicate diet collection was 534, 813, 271, 299, and
(HMDS)-facilitated diffusion (Taves, 1968) as modified 548 mL for Bauru, Brejo, Lima, Trujillo, and Pirajuí, respec-
(Whitford, 1996), with a F-ion-specific electrode (model 9409, tively. When F intake from water was considered, significant
Orion Research, Cambridge, MA, USA) and a miniature calomel differences among the communities were found (KW = 93.98,
reference electrode (Accumet #13-620-79), both coupled to a p < 0.0001). The highest amounts occurred for Brejo (0.66 ± 0.20
potentiometer (Orion, model EA 940). F standards (0.019, mg), and despite this value being almost twice as high as that
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4. 144 Rodrigues et al. J Dent Res 88(2) 2009
Table. Mean ± SD (range) F Intake from Dietary Components (solids, water, and other liquids) and Total Diet
of 4- to 6-year-old Children Receiving Systemic F from Different Sources
F Intake from Dietary Components (mg)*
Sources of F from
Systemic Other Total Diet
Community/Country F Intake Solids Water Beverages (mg/Kg b.w.) n
Bauru/Brazil Artificially F water (0.6-0.8 mg F/L)0.33 ± 0.13a 0.34 ± 0.13a 0.13 ± 0.08a 0.04 ± 0.01b 25
(0.17-0.76) (0.14-0.67) (0.01-0.28) (0.02-0.08)
Brejo dos Santos/ Naturally F water (0.6-0.8 mg F/L) 0.24 ± 0.13ad 0.66 ± 0.20a 0.15 ± 0.16a 0.06 ± 0.02ab 21
Brazil (0.05-0.51) (0.30-1.07) (0.00-0.58) (0.04-0.09)
Lima/Peru F salt (180-200 mg F/Kg) 0.75 ± 0.41b 0.04 ± 0.05b 0.11 ± 0.04a 0.05 ± 0.02ab 26
(0.17-1.72) (0.00-0.19) 0.05-0.22) (0.02-0.11)
Trujillo/Peru F milk (250 mL of 1.0 mg F/L milk) 0.63 ± 0.14b 0.13 ± 0.08cd 0.39 ± 0.09c 0.06 ± 0.01a 25
(0.39-0.91) (0.00-0.29) (0.29-0.60) (0.04-0.08)
Pirajuí/Brazil Non-F water 0.10 ± 0.07cd 0.05 ± 0.02bd 0.04 ± 0.04b 0.01 ± 0.00c 24
(0.01-0.24) (0.02-0.10) (0.01-0.22) (0.00-0.02)
KW (p) 87.49 93.98 71.93 69.16
(p < 0.0001) (p < 0.0001) (p < 0.0001) (p < 0.0001)
* Means in the same column followed by distinct superscripts indicate statistical significance among the communities (Dunn’s test, p < 0.05).
found for Bauru (0.34 ± 0.13), this difference was not signifi- latter into ‘water plus milk’ and ‘other beverages.’ This approach
cant. The lowest amounts of F intake from water were found for was successfully applied in Brazilian children (Almeida et al.,
Pirajuí (0.05 ± 0.20 mg) and Lima (0.04 ± 0.05 mg), which did 2007) and seems to be suitable for the identification of dietary
not differ significantly from each other. The F intake from water risk factors for dental fluorosis. Therefore, it was regarded
in Trujillo (0.13 ± 0.08 mg) was higher than that in Pirajuí, but as appropriate for this study, where children of different coun-
not significantly (Table). tries and communities within a country are exposed to differ-
Regarding the F intake from other beverages, there was also ent F-delivery sources. In Trujillo, the data on F intake from
a statistically significant difference among the communities milk as an isolated product were also included, due to the exist-
(KW = 71.93, p < 0.0001). The amounts found for Trujillo (0.39 ence of a milk fluoridation program.
± 0.09 mg) were significantly higher when compared with those Surprisingly, Trujillo had water F concentration rates much
from all the other communities (p < 0.001). This reflected the higher than expected, considering the milk fluoridation program
consumption of fluoridated milk. If the F intake from milk alone in this community. As a result, the mean dietary F intake in
is subtracted from the F intake from other beverages in Trujillo, Trujillo was the highest value observed. It is also important to
the amounts found (0.14 ± 0.09 mg) were similar to those point out the large variation in water F levels in Brejo. Since this
observed for the other communities. The amounts found for community has natural F in the drinking water, more constant F
Bauru, Brejo, and Lima were not significantly different, but levels would be expected. This variation may be due to the fact
were significantly higher (p < 0.01) than those found for Pirajuí that people in this community usually store the drinking water
(0.04 ± 0.04 mg) (Table). obtained from the wells for use in periods of drought. This stor-
As for the total dietary F intake, a statistically significant age may also have an impact on F intake, since it might increase
difference could be observed among the communities (KW = water F levels due to evaporation.
69.16, p < 0.0001). The highest concentrations were found for In optimally fluoridated communities, water was the most
Trujillo (0.06 ± 0.01 mg/Kg b.w.) and Brejo (0.06 ± 0.02 mg/Kg contributory factor for Bauru (42.60%) and Brejo (62.90%).
b.w.), which did not differ significantly from each other. The higher levels for Brejo could be explained by the higher
Intermediate values were found for Lima (0.05 ± 0.02 mg/Kg temperatures (mean annual temperature of 28°C, in contrast to
b.w.) and Bauru (0.04 ± 0.01 mg/Kg b.w.) The values found for 19-21°C for the other communities) and higher water intake
Pirajuí (0.01 ± 0.00 mg/Kg b.w.) were significantly lower when than in Bauru. In fact, the mean volume of water ingested per
compared with those from the other communities (p < 0.001) day in Brejo was the highest among the communities. Addition-
(Table). Seventeen children, most of them from Lima (n = 6) ally, Brejo is a rural community, where the consumption of
ingested more than 0.07 mg F/Kg b.w., a dose that has been industrialized foods, which may, in some cases, have high F
regarded as the threshold for dental fluorosis (Burt, 1992). content (Buzalaf et al., 2004b), is smaller compared with that in
Bauru.
When F intake from solids alone was considered, the com-
DISCUSSION
munities that showed high contributions of solids to total dietary
Recent studies have analyzed dietary F intake as a whole F intake were Lima (84.30%), Trujillo (54.90%), and Pirajuí
(Murakami et al., 2002; Levy et al., 2004; Franco et al., 2005; (44.80%). This result was expected for Lima, which has fluori-
Pessan et al., 2005). However, due to the high consumption of milk dated salt, but not for Trujillo. This high F-intake value may be
and water by Canadian children, Clovis and Hargreaves (1988) due to the diffusion effect of salt fluoridation in Trujillo (the
analyzed total F intake of solids and beverages, separating the distance between these communities is around 500 km). In
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5. J Dent Res 88(2) 2009 F Intake by Preschool Children 145
Trujillo, two children had a high F concentration in the salt used Bratthall D, Hänsel-Petersson G, Sundberg H (1996). Reasons for the caries
at home. Thus, it is possible that children living in Trujillo and decline: what do experts believe? Eur J Oral Sci 104:416-422.
using non-fluoridated salt at home consumed food manufac- Burt BA (1992). The changing patterns of systemic fluoride intake. J Dent
Res 71:1228-1237.
tured with fluoridated salt. Additionally, the distribution of
Burt BA, Eklund SA (2005). Dental caries. In: Dentistry, dental practice and
fluoridated salt in Peru must be monitored.
the community. Burt BA, Eklund SA, editors. St. Louis: Elsevier
Regarding the F intake from other beverages, the value Saunders, pp. 233-258.
found for Trujillo (0.39 ± 0.09 mg) was significantly higher Buzalaf MAR, Kobayashi CAN (2007). Sources of fluoride intake and risk
when compared with those from all communities, due to the of dental fluorosis. Actualizaciones en Osteologia 3:13-24.
consumption of fluoridated milk. The higher F intake from other Buzalaf MAR, Granjeiro JM, Damante CA, Ornelas F (2001). Fluoride
beverages in the fluoridated communities was anticipated and content of infant formulas prepared with deionized, bottled mineral and
may be due to the use of fluoridated water to prepare other bev- fluoridated drinking water. ASDC J Dent Chid 68:37-41.
erages, such as powdered milk (Buzalaf et al., 2001, 2004a), Buzalaf MAR, Granjeiro JM, Damante CA, Ornelas F (2002a). Fluctuations
juices, and teas (Buzalaf et al., 2002b). In previous studies con- in public water fluoride level in Bauru, Brazil. J Public Health Dent
62:173-176.
ducted in Bauru with 4- to 7-year-olds (Pessan et al., 2005), 2-
Buzalaf MAR, Bastos JRM, Granjeiro JM, Levy FM, Cardoso VES,
to 6-year-olds (Levy et al., 2004), and 1- to 3-year-olds (Almeida
Rodrigues MHC (2002b). Fluoride content of several brands of teas
et al., 2007), the dietary F intake was 0.02 ± 0.01, 0.03 ± 0.03, and juices found in Brazil and risk of dental fluorosis. Rev FOB
and 0.03 ± 0.01 mg/Kg b.w., respectively. These intakes are 10:263-267.
lower than those found for this community in the present study. Buzalaf MAR, Damante CA, Trevizani LM, Granjeiro JM (2004a). Risk of
A possible factor responsible for this difference may be the fluorosis associated with infant formulas prepared with bottled water. J
distinct age range when compared with that used in the present Dent Child 71:110-113.
study. Regarding the non-fluoridated community (Pirajuí), the Buzalaf MAR, de Almeida BS, da Silva Cardoso VE, Olympio KP, de
estimated dietary F intake was very close to levels reported Almeida Furlani T (2004b). Total and acid-soluble fluoride content of
previously (Levy et al., 2004) for 2- to 6-year-old children infant cereals, beverages and biscuits from Brazil. Food Addit Contam
21:210-215.
residing in another non-fluoridated Brazilian community (0.004
Clovis J, Hargreaves JA (1988). Fluoride intake from beverage consump-
± 0.003 mg/Kg b.w.).
tion. Community Dent Oral Epidemiol 16:11-15.
The total dietary F intake found for Trujillo and Brejo was Franco AM, Saldarriaga A, Martignon S, González MC, Villa AE (2005).
0.06 ± 0.01 and 0.06 ± 0.02 mg/Kg b.w., respectively. In Trujillo, Fluoride intake and fractional urinary fluoride excretion of Colombian
overlap of systemic fluoridation methods (naturally fluoridated preschool children. Community Dent Health 22:272-278.
water, salt fluoridation, and milk fluoridation) has probably Guha-Chowdhury N, Drummond BK, Smillie AC (1996). Total fluoride
occurred, whereas in Brejo the high F intake seemed to be related intake in children aged 3 to 4 years—a longitudinal study. J Dent Res
mainly to the high ingestion of naturally fluoridated water. For 75:1451-1457.
both communities, strategies for reducing F intake are necessary, Horowitz HS (1990). The future of water fluoridation and other systemic
since if F intake from dentifrices is added to the amounts fluorides. J Dent Res 69(Spec Iss):760-764.
Khan A, Moola MH, Cleaton-Jones P (2005). Global trends in dental fluorosis
obtained from the diet, it is probable that the upper limit of F
from 1980 to 2000: a systematic review. S Afr Dent J 60:418-421.
intake (0.07 mg/Kg b.w./day) (Burt, 1992) is exceeded for many
Kumar JV, Moss ME (2008). Fluorides in dental public health programs.
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in Trujillo, indicates that decision-making for the boundaries of Levy FM, Bastos JRM, Buzalaf MAR (2004). Nails as biomarkers of fluo-
national programs of community water fluoridation cannot dis- ride in children of fluoridated communities. J Dent Child 71:121-125.
regard political, cultural, and geographical differences within Marthaler TM (2004). Changes in dental caries 1953-2003. Caries Res
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temic method of fluoridation is implemented; and (b) F exposure Prospective study of the association between fluoride intake and dental
monitoring of existing and newly developed fluoridation schemes fluorosis in permanent teeth. Caries Res 42:125-133.
McDonagh MS, Whiting PF, Wilson PM, Sutton AJ, Chestnutt I, Cooper J,
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et al. (2000). Systematic review of water fluoridation. BMJ 321:855-859.
Murakami T, Narita N, Nakagaki H, Shibata T, Robinson C (2002). Fluoride
ACKNOWLEDGMENTS intake in Japanese children aged 3-5 years by the duplicate-diet tech-
nique. Caries Res 36:386-390.
This study was supported by The Borrow Foundation. The National Health and Medical Research Council (2007). A systematic review
authors thank CAPES for a PhD scholarship to the first author. of the efficacy and safety of fluoridation. Reference #EH41. Canberra,
This study was based on a thesis submitted to Bauru Dental Australia: NHMRC Publications (available for download only).
School, University of São Paulo (Brazil), in partial fulfillment Paiva SM, Lima YB, Cury JA (2003). Fluoride intake by Brazilian children
of the requirements for the PhD degree in Oral Biology. from two communities with fluoridated water. Community Dent Oral
Epidemiol 31:184-191.
Pessan JP, Pin ML, Martinhon CC, de Silva SM, Buzalaf MAR (2005).
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