strontium concentrations and isotope ratios in enamel of healthy and carious teeth in southern...

Research Article

Received: 20 February 2013 Revised: 26 May 2013 Accepted: 3 June 2013 Published online in Wiley Online Library

Rapid Commun. Mass Spectrom. 2013, 27, 1919–1924

Strontium concentrations and isotope ratios in enamel of healthyand carious teeth in southern Shaanxi, China

Zixia Li1,2,3†, Maoyong He2*,†, Bin Peng1**,† and Zhangdong Jin2

1Department of Conservative Dentistry and Endodontics, School of Stomatology, Wuhan University, Wuhan 430079, China2State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environment, Chinese Academy of Sciences, Xi'an710075, China3Department of Stomatology, Xi'an Medical University, Xi'an 710021, China

RATIONALE:As the trace element strontium (Sr) plays a significant role in dental health, it is important to determine theSr concentration and isotope composition (87Sr/86Sr) of teeth and whether these values are related to caries formation,age and sex.METHODS: A total of 160 permanent teeth were collected from 7- to 79-year-old people from the southern Shaanxi areaof China, including 100 healthy teeth and 60 carious teeth (men and women each accounted for half of the samples). Theconcentration and isotope composition of Sr elements in the dental enamel of the teeth were measured using inductivelycoupled plasma mass spectrometry (ICP-MS) and thermal ionization mass spectrometry (TIMS).RESULTS: A significantly lower Sr concentration was found in the enamel of the carious teeth than in that of the healthyteeth for individuals of varying ages and sex. The Sr concentration in human carious teeth ranged between 79.70 μg/gand 85.80 μg/g; while the Sr concentration in healthy teeth ranged between 128 μg/g and 156.77 μg/g. Our results alsodemonstrated that the 87Sr/86Sr ratio did not appear to be affected by the caries formation, age or sex. The 87Sr/86Sr ratioin the enamel of the healthy and carious teeth of individuals of varying ages and genders ranged between 0.710935 and0.711037, which falls into the range of 87Sr/86Sr ratios found in the local, naturally occurring water, soils and rocks.CONCLUSIONS: Sr plays a significant role in dental health, and there is a negative correlation between Sr and theoccurrence of dental caries. The 87Sr/86Sr ratio of teeth reflects the 87Sr/86Sr ratio of the associated environment, and thereis no significant relationship with the frequency of dental caries, age or sex. Copyright © 2013 John Wiley & Sons, Ltd.

(wileyonlinelibrary.com) DOI: 10.1002/rcm.6646

Trace elements play an important and complex role in thehuman metabolism and, although present in only minuteconcentrations, can be either beneficial or detrimental tohealth. Biomonitoring of trace elements in human teeth hasbecome an important tool to evaluate the nutritional andenvironmental status of an individual.[1–4]

With the improvement in personal living conditionstandards, food processing has become increasinglysophisticated. The incidence of associated dental caries hasalso grown, reaching 60–70% in China with rates as high as90% in some areas.[5] Therefore, finding new ways to preventand treat dental caries has become critical. Manyepidemiological investigations, animal experiments, and

* Correspondence to: M.-Y. He, State Key Laboratory of Loessand Quaternary Geology, Institute of Earth Environment,Chinese Academy of Sciences, Xi'an 710075, China.E-mail: [email protected]

** Correspondence to: B. Peng, Department of ConservativeDentistry and Endodontics, School of Stomatology, WuhanUniversity, Wuhan 430079, China.E-mail: [email protected]

† These authors contributed equally to this study.

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model experiments have proven that the trace element Srplays a significant role in dental health and have found anegative correlation between Sr and the occurrence of dentalcaries.[6–12] However, there have been few reports about theaverage Sr content in carious or healthy teeth and any linkbetween Sr levels in human tooth enamel and caries, ageand sex. The Sr isotopic composition (i.e., 87Sr/86Sr ratio) ofan animal's bones and teeth directly reflects the 87Sr/86Sr ratioof its environment. Thus, analysis of the Sr component ofvertebrate skeletal material has several applications inpalaeoecological and palaeobiological research.[13–20]

Building on the principles of strontium isotope geochemistry,archaeologists have used the radiogenic strontium isotopesignatures in human enamel apatite to reconstruct ancientmobility patterns and to distinguish between individuals oflocal and non-local origins at archaeological sites. The datapresented here contribute some reference values forresearchers interested in past populations, especially as therehas not been much of this data published for China.

In this study, we measured the trace element Srconcentrations and 87Sr/86Sr isotope ratios in the enamel ofhealthy and carious teeth from residents of the southernShaanxi Province, China, and determined the 87Sr/86Srisotope ratios for drinking water, soil and rocks in the sameregion. The purpose of this research was to answer thefollowing questions.

Copyright © 2013 John Wiley & Sons, Ltd.

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(1) Are Sr levels in human tooth enamel linked to caries, ageand sex?

(2) Does the 87Sr/86Sr ratio vary between healthy and cariousteeth?

(3) Is the 87Sr/86Sr ratio linked to caries, age and sex?

EXPERIMENTAL

Instruments

A pressurized microwave digestion device (Ethos TouchControl, Shelton, CT, USA), which provided 800 W ofmicrowave energy with a frequency of 2450 MHz at fullpower with a rotor for 12 Teflon digestion vessels, was usedto digest the samples of tooth enamel.A model 7700x mass spectrometer (Agilent Technologies,

Tokyo, Japan), fitted with a standard glass concentricnebulizer, quartz double-pass spray chamber, nickel samplerand skimmer cones, was used for the inductively coupledplasma mass spectrometry (ICP-MS) analyses.[21] Theoperating conditions used for the analysis of samples areshown in Table 1.Isotopic measurements were performed on an IsoProbe-T

thermal ionization mass spectrometer (GV Instruments Ltd,Manchester, UK). The instrument is equipped with nineFaraday cups, seven Channeltron ion counters, one Dalydetector and one ETP electron multiplier.A Milli-Q ultrapure water system (Millipore Co., Billerica,

MA, USA) was used to provide the ultrapure water(18.2 MΩ) used for the experiments.[21]

Reagents

Nitric acid (HNO3, guarantee reagent (GR)) and hydrogenperoxide (H2O2, 30%) were utilized.The standard material for the Sr isotope, NBS987, was

obtained from the National Institute of Standards andTechnology (NIST, Gaithersburg, MD, USA). The HCl andHNO3 used in the experiment were both purified with aDST-1000 double-bottle sub-boiling distillation device(Savillex Co., Eden Prairie, MN, USA). All experiments wereperformed in an ultra-clean chemical laboratory.

Table 1. Agilent 7700x ICP-MS instrument operatingconditions for the analysis of samples

Parameter ValuePlasma mode Normal, robustRF forward power (W) 1500Sampling depth (mm) 8.2Carrier gas flow rate (L/min) 1.26Dilution gas flow rate (L/min) 0.4Spray chamber temperature (°C) 2Extraction lens 1 voltage (V) 0Kinetic energy discrimination voltage (V) 4He cell gas flow rate (mL/min) 4Diameter of sampling cone hole (mm) 1.0Diameter of skimming cone hole (mm) 0.4

wileyonlinelibrary.com/journal/rcm Copyright © 2013 John Wil

Acquisition of the samples

Teeth extracted from local long-time residents of the southernShaanxi Province, China, were collected. The healthy teethwere extracted from sample providers who did not smokeor drink. The teeth were healthy permanent teeth extracteddue to impacted wisdom tooth deformity, orthodontictreatment, or other reasons. Extracted teeth with completecrowns, no caries or mottled enamel, complete enameldevelopment, and no obvious wear or defects on the morsalsurface were selected. The selected carious teeth exhibitedclear cavities. A total of 160 permanent teeth were collectedfrom 7- to 79-year-old people from the southern Shaanxi areaof the China, including 100 healthy teeth and 60 carious teeth(men and women each accounted for half of the samples). Theextracted teeth were divided into five groups according to theages of the sample providers, with each group containing tenteeth each from male and female contributors.

Drinking water samples were collected from rivers,reservoirs and wells. Before water sample collection, thewater temperature and pH were measured at each site. Thewater samples were in situ filtered on collection through0.2-μm Whatman nylon filters.

In addition, soil and rocks in this region were collectedfollowing the method established by Harb et al.[22] A total of 8rocks and 10 surface soil samples were collected randomly fromthe study area. Rock samples were crushed into small pieces andground to a powder. Soil samples were collected, with the onlyconstraint being that no sampling site should be taken close toa field boundary, a road, a tree or other obstruction. Surface soilswere then taken from different places randomly within themarked and cleared area from the ground surface up to 2 cmand mixed together thoroughly in order to obtain a represen-tative sample of that area. Each sample (rock/soil) was dried inan oven at 105 °C and sieved through a 100 mesh sieve whichis the optimum size for samples enriched in heavy metals.

Treatment of teeth

The acquired teeth were first rinsed with Milli-Q water toremove the blood from the surface and were soaked in agrinding mouth glass bottle in an acetone solution for 24 h.A scalpel was used to carefully scrape the organics (includingsoft tissue) from the tooth surfaces, and the samples werewashed with Milli-Q water and ethanol. The samples werethen dried and numbered. A heating percussion methodwas applied to separate the enamel from dentin of theteeth.[23] The separated enamel was collected and ground to200 mesh with an agate mortar and pestle.

A sample of 0.05 g of ground enamel was accuratelyweighed in a microwave digestion tank to which 5 mL 50%HNO3 solution and 2 mL 30% H2O2 solution were added.The tank was then gently shaken. Approximately 2 mLMilli-Q water was added dropwise, and the sample wasdigested using 1000-W microwave radiation. Thetemperature procedure of the microwave digestion was asfollows: increase from room temperature to 120 °C over5 min, maintain at 120 °C for 3 min, increase to 220 °C over8 min, and maintain at 220 °C for 15 min until the digestionwas completed. The conditions for these digestions are givenin Table 2. Finally, the vessels were cooled, carefully opened,and digests were quantitatively transferred into 25-mL

ey & Sons, Ltd. Rapid Commun. Mass Spectrom. 2013, 27, 1919–1924

Table 2. Microwave digestion programs for teeth

Program/reagents StageTime(min)

Temperature(°C)

Power(W)

5 mL HNO3 (50%),2 mL H2O2 (30%)

1 5 0-120 10002 3 120 10003 8 120-220 10004 15 220 1000

Table 4. 0.2 mL Sr-Spec (50–100 mesh) columns for Srseparations

Stage Column procedure:

1 clean resin 3 mL Milli-Q water2 precondition column 3 mL 3.5 N HNO33 load sample dissolved in 0.2 mL

3.5 N HNO34 wash 0.1 mL 3.5 N HNO35 wash 0.1 mL 3.5 N HNO36 wash 0.1 mL 3.5 N HNO37 wash 0.5 mL 3.5 N HNO38 wash 0.5 mL 3.5 N HNO39 wash 2.5 mL 3.5 N HNO310 elute Sr 3 mL warm 0.05 N HNO3

Sr concentrations and isotope ratios in teeth enamel

calibrated flasks. A vessel containing the same acid mixtureused for the samples was adopted for controlling theanalytical 'blank'.The reference materials of bone ash (NIST SRM 1400) and

bone meal (NIST SRM 1486) were simultaneous analyzedfor quality control requirements.

Treatment of soil and rocks

The soil and rock samples were dissolved using themicrowave digestion system. Soil and rock samples of0.25 g by weight were placed into a PFA (polyfluoroalkoxypolymer) vessel and 4.5 mL HCl and 1.5 mL HNO3 wereadded for Method 1. For Method 2, 4 mL HNO3, 2.5 mLHCl and 1 mL HF were added to the same weight of sample.The vessels were closed and placed into a rotor segment,which was tightened using a torque wrench. The segmentwas then inserted into a microwave cavity connecting thetemperature and pressure sensors. The conditions for thesetwo programs are given in Table 3. Finally, the vessels werecooled and carefully opened, and the digests werequantitatively transferred into 50-mL calibrated flasks.The reference materials were analyzed simultaneously for

quality control requirements.

Separation and enrichment of Sr by ion exchange

Sr in the tooth, water, soil and rocks samples was separatedfrom other cations using 0.2-mL columns filled withEichrome Sr-Spec resin (Eichrome Laboratories, Lisle, IL,USA) and eluted with ultrapure H2O.[24–31]

Unlike an ordinary cation-exchange resin, the Sr-Specselective resin significantly reduces resin use and acidleaching, thus improving the separation efficiency. This resincan achieve a complete separation of the Sr from the Ca andRb in the stroma.[24–26]

The detailed experimental methods are listed in Table 4.

Table 3. Microwave digestion methods 1 and 2 for soiland rock

Program/reagents Stage

Time(min)

Temperature(°C)

Power(W)

4.5 mL HCl,1.5 mL HNO3

1 10 200 5002 15 200 500

4 mL HNO3,2.5 mL HCl,1 mL HF

1 6 160 5002 4 210 5003 20 210 500

Copyright © 2013 JRapid Commun. Mass Spectrom. 2013, 27, 1919–1924

Mass spectrometric measurements of the Sr isotopes

The samples were analyzed by thermal ionization massspectrometry (TIMS) on a GV IsoProbe-T mass spectrometer(IsotopX, Middlewich, UK) operated in dynamic mode. Thepurified samples were dried with a drop of 0.15 M H3PO4.The dried samples were then resuspended in a mixedTaCl5/H3PO4 solution.

[24–31] Finally, the samples were loadedon degassed rhenium (Re) filaments for analysis by TIMS inthe dynamic mode with a target intensity of 3 V 88Sr. All datawere corrected for internal mass bias using 86Sr/88Sr = 0.1194.The analyses were referenced against NBS SRM 987(0.710250), with long-term averages of 0.710246 and0.710240 and 2σ internal precisions of 0.000016 and 0.000014on the IsoProbe.

RESULTS AND DISCUSSION

Sr content in the enamel of healthy and carious teeth

Figure 1 presents the Sr content values for the enamelsamples obtained by solution mode ICP-MS analysis. Theresults indicate that, although the tooth samples were

Figure 1. Sr content in the tooth samples (each group has 10samples).

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Figure 2. 87Sr/86Sr ratios in the tooth samples (each grouphas 10 samples).

Figure 3. 87Sr/86Sr ratios of the representative samples fromlocal water, soils and rocks.

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acquired from individuals of different sexes and ages, the Srconcentrations were significantly lower in the carious teeththan in the healthy teeth. The Sr content ranged from128 μg/g to 156.77 μg/g for the healthy teeth and from79.70 μg/g to 85.80 μg/g for the carious teeth. The results ofour experiments are similar to those previously reported byCurzon[6] and Riyat and Sharma.[10] It was suggested thatthe average Sr content in healthy teeth is 86.38 μg/g and thatthe Sr content in the carious teeth was below this value. Theseresults are in agreement with previous reports regarding theexistence of a relationship between Sr content of enamel anddental health.Figure 1 also shows the comparison of mean levels of Sr

concentrations in enamel by sex and age. The difference inSr concentration between males and females was significant(p <0.01), with the concentration being higher in females thanin males. Kumagai et al. reported that females often exhibithigher Sr/Ca ratios than males, a fact usually attributed tolower meat intake among women.[4] However, more samplesand further research are required to clarify the reason for thisin Chinese women. The results of the present study showedthat Sr concentration in enamel changed with age: increasingfrom 7 years to 40 years, and then decreasing from 40 years to80 years or older. This is considered to be because enamelcontains a large amount of collagen fibers and that, as theelements which have an affinity for collagen fiber areabsorbed in the body and the cumulative dosage increases,the Sr concentrations rise with age. After the age of 40 yearsthere is loss of the collagen fibers and thus a correspondingdecrease in the Sr concentration. The results of ourexperiments are in agreement with those in previous reportsby Kumagai et al.,[4] Brown et al.,[32] and Arruda-Netoet al.[33] As significant differences in Sr concentrations wereobserved between the sexes and positive correlations wereobserved between Sr concentrations and age, this suggests thatin all future experiments that use the elemental composition ofhuman primary teeth as environmental indicators, it will benecessary at least to control for age and sex.The significance of the trace elements, other than fluoride, on

the development of dental caries is of interest in dentalresearch. Among theses elements, strontium has been referredto as a possible cariostatic agent, based on evidence from anumber of experimental and epidemiological studies. Morethan 96% of tooth enamel consists of inorganics, primarilycalcium phosphate hydroxyapatite. The chemical propertiesand atomic radius of Sr are similar to those of Ca. During theprocess of tooth formation, Sr ions can substitute for Ca ionsin the hydroxyapatite crystal lattice to yield a typical Sr contentof up to 50–400 μg/g in the enamel of adults. There are threepossible mechanisms for Sr having an anti-caries effect.

(1) An increase in the size of the hydroxyapatite crystals canreduce the surface of the crystal, rendering it difficult todissolve.

(2) The Sr could form a cladding layer on the surface of thehydroxyapatite crystals, thus reducing their solubility orthe acid-soluble speed of the enamel. The followingSr-bearing apatites could be formed depending on thesolutionmedia: (Ca)6(Sr)4(PO3)6(OH)2, (Ca)6(Sr)4(PO3)6(F)2.

(3) The Sr could inhibit bacterial growth and reduce acidproduction or combinewith cariogenic bacteria and surfaceglaze to inhibit the pH reduction caused by sugars.


87Sr/86Sr ratios in the enamel of healthy and carious teeth

Using the previously described experimental procedures, theSr isotopes in the enamel of the extracted teeth, the water, soiland the rock samples were chemically separated andmeasured. The measurement results are shown in Figs. 2and 3. The data in Fig. 2 indicate that the median 87Sr/86Srratio in the enamel of the healthy teeth from the southernShaanxi Province, China, ranged from 0.710948 to 0.711037,and the median 87Sr/86Sr ratio in the enamel of the cariousteeth ranged from 0.710935 to 0.711034. Figure 3 shows thatthe 87Sr/86Sr ratio of the representative water sources in thestudy area was between 0.710497 and 0.710991, the 87Sr/86Srratio of the representative rocks was between 0.707715 and0.711484, and the 87Sr/86Sr ratio of the representative soilswas between 0.706742 and 0.711883.

The data in Fig. 2 indicate that the 87Sr/86Sr ratio in theenamel of the healthy and carious teeth fluctuated over anarrow range and was generally stable, without significantvariation with respect to age and gender. The data in Fig. 3also indicate that the 87Sr/86Sr ratio in the enamel of thehealthy and carious teeth varied from 0.710935 to 0.711037,which is within the range of the 87Sr/86Sr ratios (0.706742 to0.711883) found in natural water and rocks.

Because its chemical behavior and atomic radius are similarto those of calcium, strontium commonly substitutes forcalcium in the crystalline lattice of hydroxyapatite in teeth.Numerous previous investigations have demonstrated the


Sr concentrations and isotope ratios in teeth enamel

effective use of strontium isotope analysis of human tissue(e.g., bone, teeth) as an important tool for examining ancienthuman migration. This technique is particularly effective inregions of the world where the 'background' Sr isotopesignatures are sufficiently varied as an indicator ofdifferences between potential places of origin.[13–20]

Strontium present in rock, soil and ground-water isincorporated into local plants and animals, and hence the Srisotopic composition of an individual's diet will be reflected inhis or her hard tissues. The strontium concentration of plantor animal tissue will vary according to its trophic position.However, the isotopic composition of strontium is not changedor fractionated by biological processes during strontiumtransport through the ecosystem, because the mass differencesbetween the four strontium isotopes are relatively small.The results of this experiment support the use of Sr isotopes

for studying the habitats of ancient populations. For humansor animals living in a particular geological region, the Srisotope ratio in the body is close to that in the environment.The results of this experiment further confirmed this theoryand verified the reliability of the measurement methodsutilized in the study.

CONCLUSIONS

Using ICP-MS and TIMS, the concentration and isotopecomposition of Sr elements in the dental enamel from humanteeth collected from the southern Shaanxi area of the Chinawere precisely measured. The results of the experimentsindicated the following:

(1) The Sr concentrations in human tooth enamel weresignificantly lower in carious teeth than in healthy teeth.The Sr concentration was higher in females than in males.The Sr concentration in enamel changed with age,increasing from 7 years to 40 years, and then decreasingup to 80 years or older.

(2) The 87Sr/86Sr ratios in human tooth enamel were similarand exhibited no significant relationship with thefrequency of dental caries, age or sex. The 87Sr/86Sr ratioin the enamel of the healthy and carious teeth fluctuatedover a narrow range and was generally stable.

AcknowledgementsThis work was supported by the National Natural ScienceFoundation of China (Nos. 41103008 and 40976074) and bythe State Key Laboratory of Loess and Quaternary Geologythrough grant SKLLQG1114 and by the Foundation ofInstitute of Earth Environment, Chinese Academy of Sciences(IEECAS 2012). We are grateful to the anonymous reviewersfor numerous suggestions on an earlier version; thesesubstantially improved this manuscript.

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