10.59987/ads/2014.2.41-51
Aims. The aim of this research is to verify the quality and quantity of heavy metals (HM) of dental origin in TMD patients. Methods. A population of 100 subject was studied and divided in two homogeneous groups: Study Group (SG) and Control Group (CG). Organism heavy metals were tested by a spot sampling method in which the first urine of the day, through Inductively Coupled Plasma-Mass Spectrometry (ICP-MS), were analyzed. The results obtained were compared with reference values (RV) of Italian people. Descriptive statistical analysis and student's t-test has been applied (statistical significance for p &gt; 0.05).
Results. The SG presented the absolute highest levels of HM compared to the CG (p=0.787). As regards the relation between pain and HM, the subjects that refer “severe/very severe” values of pain present the highest levels of HM in urines.
Conclusions. The obtained results seem to highlight a possible direct proportionality between the level of pain the increase of the concentration of heavy metals in all the examined groups and subgroups.
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Annali di stomatologia
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Heavy metals and pain in the dysfunctional patient
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Heavy metals and pain in the dysfunctional patient
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                                                                                                 Original article



    Heavy metals and pain in the dysfunctional patient




                                                                                                                   li
                                                                   na
    Carlo Di Paolo, MD, DDS                                 idea that inflammation might be a pivotal factor in the
    Emanuela Serritella, DDS                                pathogenesis of such disorders. Other authors (5,6)




                                                                 io
    Fabrizio Panti, MD                                      claim that the production of free radicals, pro-inflam-
    Giovanni Falisi, DDS, PhD                               matory and others neuropeptides, may lead to local-
    Fedele Manna, SSD                                       ized inflammation, chronic tissue modifications, and
                                                            to the development of neurogenic sensitization.




                                                              az
                                                            Toxins, free radicals and metals can caused inflam-
    Department of Oral and Maxillo-facial Sciences          mation phenomena and cellular homeostasis modifi-
    Sapienza University of Rome, Italy                      cations, generating pathologies and sometimes even
                                                            irreversible damages (7-13). Among these, heavy




                                                           rn
                                                            metals are particularly relevant. They can penetrate
    Corresponding author:                                   the organism through numerous ways (food, medi-
    Emanuela Serritella                                     cines, cosmetics), including materials routinely used
    Via Caserta, 6                                          in dentistry, leading to a deficiency in some vital func-




                                                        te
    00161 Rome, Italy                                       tions (14-18).
    E-mail: emanuela.serritella@gmail.com                   An elevated concentration and accumulation of free
                                                            radicals in biological tissues may cause oxidative

    Summary
                                                     In     stress (19-24). Among heavy metals, Mercury (Hg),
                                                            deriving from alimentary, iatrogenic, cosmetic factors
                                                            and mostly from amalgam dental fillings, can cause a
    Aims. The aim of this research is to verify the         particularly relevant chronic intoxication (17,25).
    quality and quantity of heavy metals (HM) of den-       The aim of this research is to quantify the quality and
                                                ni
    tal origin in TMD patients. Methods. A population       quantity of heavy metals of dental origin in TMD pa-
    of 100 subject was studied and divided in two ho-       tients. This comparison is based on the possible rela-
    mogeneous groups: Study Group (SG) and Con-             tionship between these pathological conditions and
    trol Group (CG). Organism heavy metals were             the inflammatory processes. This research project re-
                              o

    tested by a spot sampling method in which the           quires the comparison between three groups of ran-
    first urine of the day, through Inductively Coupled     domly selected subjects: a group of dysfunctional pa-
                          izi


    Plasma-Mass Spectrometry (ICP-MS), were ana-            tients with metal manufacts in the oral cavity, a group
    lyzed. The results obtained were compared with          of dysfunctional patients without any metals and a
    reference values (RV) of Italian people. Descrip-       group of non-dysfunctional subjects, without any met-
    tive statistical analysis and student's t-test has      als in the oral cavity.
           Ed




    been applied (statistical significance for p > 0.05).
    Results. The SG presented the absolute highest
    levels of HM compared to the CG (p=0.787). As re-       Materials and methods
    gards the relation between pain and HM, the sub-
    jects that refer “severe/very severe” values of         A consecutive series of patients has been selected,
    pain present the highest levels of HM in urines.        all spontaneously joining the Service of Clinical
    C




    Conclusions. The obtained results seem to high-         Gnathology of the Department of Odontostomatologi-
    light a possible direct proportionality between the     cal and Maxillofacial Sciences of the University of
CI




    level of pain the increase of the concentration of      Rome “Sapienza”, from February 1 st to November
    heavy metals in all the examined groups and sub-        30th 2011, for a total of 200 patients. These were di-
    groups.                                                 vided into two groups: a Study Group (SG) and a
                                                            Control Group (CG), according to the correspon-
    Key words: heavy metals, pain, TMD.                     dence to the following criteria:
                                                            Inclusion criteria for the Study Group: 1. Presence of
©




                                                            TMD belonging to groups I, II, III of the Axis I, accord-
    Introduction                                            ing to the RDC/TMD classification, or problems of ar-
                                                            ticular dysfunction related to all phases of condylo-
    Temporomandibular Disorders (TMD) are a group of        discal incoordination, from mandibular dislocation to
    pathologies determined by an interaction of structur-   arthrosis, 2. Presence of one or more conservative or
    al, psycho-socio-environmental and genetic elements     prosthetic metal manufacts, minimum 2 amalgam fill-
    (1,2). In the past some authors (3,4) developed the     ings and/or 1 fixed-removable prosthesis.

    Annali di Stomatologia 2014; V (2): 41-51                                                                     41
    C. Di Paolo et al.


    Inclusion criteria for the Control Groups: The study          randomly, using a spot sampling according to Araki S.’
    provides the composition of two control groups, 1 and         method, and providing patients with a sterile 50cc con-
    2. The first (CG1) is made up of TMD patients with            tainer to collect early morning urines, which has been
    the above mentioned characteristics who do not pre-           then returned to the Service of Clinical Gnathology.
    sent any conservative or prosthetic metal manufacts           Urines analysis: urines have been analyzed by the




                                                                                                                            li
    inside the oral cavity. The second (CG2) is made up           Laboratory of Geochemistry of the Department of
    of healthy subjects without any conservative or pros-         Earth Sciences of the University of Rome “Sapienza”.




                                                                      na
    thetic metal manufacts inside the oral cavity.                Analytical data have been elaborated in cooperation
    Exclusion criteria for all the groups: 1. Positivity to the   with the Department of Chemistry and Medicine
    Axis II of the classification RDC/TMD 2. Occurrence           Technologies of the University of Rome “Sapienza”.
    of well-known local and/or systemic diseases that             The assay of the heavy metals present in dental al-




                                                                    io
    may alter the inflammatory condition of the examined          loys, named “ODmetals” (Tab. 3), has been per-
    subjects. 3. Presence of other metals in the body. 4.         formed, as well as of other toxic metals, for a total
    Subjects who do not accept to be part of the survey.          number of 22 metals examined (Tab. 4), also to test
    Suitable patients for the research are in the number of       the subjects’ degree of intoxication.




                                                                 az
    50 for the Study Group and 15 for the Control Group.          A measurement of the relative density has been car-
    The scarce number of dysfunctions in this last group          ried out through a refractometer, in order to correct
    indicates the difficulty in finding patients without any      the results according to Araki S’method (26). The
    prosthetic or conservative reconstructions among the          samples have then been analyzed through the ICP-




                                                              rn
    subjects affected by TMD. Thus, in order to have an           MS mass spectrometry (Inductively Coupled Plasma-
    equal number of participants in the two groups, 35            Mass Spectrometry). Data interpretation is possible
    subjects have been recruited in the Control Group             by confrontating the results with the reference values




                                                           te
    among the medical and the nursing staff of the Ser-           (RV) for Italy (Tab. 5), elaborated by the National In-
    vice and students from the degree course in “Dental           stitute for Health (ISS) of Rome, that measures the
    Sciences” at the University of Rome “Sapienza”.               presence of metals in the Italian population between
    The total patient population is thus made up of 100           1990 and 2009 (27).

    male sex, 50 belonging to the Study Group (SG) and
                                                        In
    subjects, of an average age of 41, mainly from the fe-        These values have been compared with those resulting
                                                                  from the analysis of the collected samples, in order to
    50 to the Control Group (CG). (Tab. 1-2)                      check if they were normal. The research on the possi-
    The SG is made up of TMD-affected patients, whose             ble correlation between the presence of heavy metals
    level of heavy metals has been evaluated and com-
                                           ni
    pared with the intensity and typology of the dysfunc-
    tional pathology; the CG, 50 subjects without any             Table 3. OD METALS.
    metals in the oral cavity, is made up of 15 dysfunc-
    tional patients (CG1) more 35 non-dysfunctional sub-          Heavy metals of dental origin
                             o

    jects (CG2). The CG1 has been compared with the               Manganese (Mn)
    SG to evaluate the relationship between heavy met-            Copper (Cu)
                         izi


    als, intensity and dysfunctional typology.                    Zinc (Zn)
    All the subjects involved have been informed in ad-           Molybdenum (Mo)
    vance about the study, its aims and the potential risks,      Cobalt (Co)
    and have been given an informed consent paper. All            Tin (Sn)
           Ed




    have undergone a health checkup, consisting of a gen-         Nickell (Ni)
    eral medical examination performed by a specialist (an        Mercury (Hg)
    anesthetist), and requiring basic hemato-chemical ex-         Antimony (Sb)
    aminations in order to highlight the absence of any in-       Indium (In)
                                                                  Titanium (Ti)
    progress inflammation. The study has been carried out
    C




    Table 1. Distribution of age in SG e CG.
CI




    AGE                         SG                      CG        Table 4. Heavy metals examined.
    Minimum                     23                      22
    Maximum                     75                      62        • Aluminum (Al)                          • Colbalt (Co)
    Mean                        47,92                   28,59     • Iron (Fe)                              • Cadmium (Cd)
    Median                      51,5                    27,5      • Manganese (Mn)                         • Tin (Sn)
                                                                  • Copper (Cu)                            • Nickel (Ni)
©




                                                                  • Arsenic (As)                           • Lead (Pb)
                                                                  • Cesium (Cs)                            • Mercury (Hg)
    Table 2. Distribution of gender in SG e CG.
                                                                  • Lithium (Li)                           • Antimony (Sb)
                                                                  • Rubidium (Rb)                          • Indium (In)
    GENDER                       SG                     CG
                                                                  • Zinc (Zn)                              • Titanium (Ti)
    Female                       39                     31        • Strontium (Sr)                         • Barium (Ba)
    Male                         11                     19        • Molybdenum (Mo)                        • Uranium (U)


    42                                                                                Annali di Stomatologia 2014; V (2): 41-51
    Heavy metals and pain in the dysfunctional patient


     Table 5. Concentration of metals in the urine for the Italian population from 1990 to 2009.

          Metal                      Reference value (RV)                                    Other studies
                                           Urine (µg/L)                                Average ± ds Urine (µg/L)




                                                                                                                          li
                                                                         10,9±1,06 (AAS, ICP-AES 1990)
            Al           2,3-19,5 (1990)
                                                                         5,36±3,76 (ICP-MS 2009)




                                                                        na
            As           2,3-31,1 (1990)                                 16,7±1,9 (AAS, ICP-AES, NAA 1990 )
                                                                         0,86±0,06 (AAS, ICP-AES 1990
            Cd           0,38-1,34 (1990)
                                                                         0,81±0,53 (ICP-MS 2009)
                                                                         0,57±0,1 (AAS, ICP-AES, NAA 1990)
            Co           0,18-0,96 (1990)




                                                                      io
                                                                         0,24±0,18 (ICP-MS 2009)
                                                                         8,1±1,5 (NAA 1990)
                         0,1-17,5 (1990)
            Cs                                                           4,52±2,24 (ICP-MS 2005)
                         2,00-6,82 (2005)




                                                                   az
                                                                         12,9±8,3 (ICP-MS 2009)
                                                                         23±6,9 (AAS, ICP-AES, NAA 1990)
            Cu           4,20-50 (1990)
                                                                         12,9±7,0 (ICP-MS 2009)
            Fe                                                           8,70±6,27 (ICP-MS 2009)




                                                                rn
                                                                         3,5±0,2 (AAS, ICP-AES, NAA 1990)
            Hg           0,1-6,9 (1990)
                                                                         1,92±1,60 (ICP-MS 2009)
            Li                                                           17,3±13,6 (ICP-MS 2009)
                                                                         1,02±0,05 (AAS, ICP-AES 1990)




                                                             te
            Mn           0,12-1,90 (1990)
                                                                         0,22±0,10 (ICP-MS 2009)
            Mo                                                           36,9±16,9 (ICP-MS 2009)
                                                                         0,9±0,11 AAS, (ICP-AES 1990)
            Ni           0,06-1,74 (1990)
                                                          In             0,87±0,50 (ICP-MS 2009)
                                                                         17 ± 0,46 (AAS, ICP-AES 1990)
            Pb           12,0-27,0 (1990)
                                                                         1,80 ± 1,40 (ICP-MS 2009)
            Rb           284-4.096 (1990)                                2.190 ±203 (NAA 1990)
            Sn                                                           0,90±0,64 (ICP-MS 2009)
                                                ni

            Sr                                                           154±91 (ICP-MS 2009)
                                                                         456±58 (AAS, ICP-AES, NAA 1990)
            Zn           266-846 (1990)
                                                                         356±236 (ICP-MS 2009)
                              o

                                                                         2,7±0,5 (AAS, ICP-AES, NAA 1990)
            Ba           0,67-3,68 (2005)                                1,77±1,30 (ICP-MS 2005)
                          izi


                                                                         1,24±0,78 (ICP-MS 2009)
            In                                                           < 0,15 (NAA 1990)
                         0,19-1,10 (1990)                                0,79±0,07 (AAS, ICP-AES, NAA 1990)
            Sb
           Ed




                         0,02-0,12 (2005)                                0,07±0,04 (ICP-MS 2005)
                         0,07-0,7 (1990)                                 0,42±0,09 (AAS 1990)
            Ti
                         0,02-0,17 (1994)                                0,07±0,03 (ICP-MS 1994)
            U                                                            < 0,1 NAA (1990)
    C




    over the threshold levels and the algic symptomatology           II. Main symptoms: TMJ pain (IIIa), and MUSCULAR
    in dysfunctional patients, has been focused mainly on            pain (MM).
CI




    the Study Group, where the totality of the patients is af-       Pain has been measured with the subjective Verbal
    fected by TMD. Subsequently, the results have been               Numeric Scale (VNS), according to an index of seri-
    confronted with the symptomatology of the CG1 pa-                ousness subdivided in four categories: mild (<30);
    tients, representing 30% of the whole sample.                    moderate (30-50); severe (50-70); very severe (>70).
    The following pathological and symptomatic aspects               III. Comorbidity: among the possible co-morbidities
    have been considered:                                            with TMD, the most frequently considered are
©




    I. Articular problems: according to the RDC/TMD                  headache and cervicalgia, anamnestically described
    classification, the pathologies I, IIa, IIb, and IIIc (Axis      by patients, measured with the VNS scale and subdi-
    I) have been taken into account (1). These have been             vided with reference to the above described index of
    considered either mild or severe according to the                seriousness.
    presence or absence of pain, classified as below, and            Heavy Metals analysis: evaluates the quantity and
    to the level of chronicity, through the relation between         the typology of those metals presenting higher values
    onset time/clinical observation time.                            than the RV for the Italian population, paying particu-

    Annali di Stomatologia 2014; V (2): 41-51                                                                            43
    C. Di Paolo et al.


    lar attention to the most frequent heavy metals in            cant for the aims of this research have been reported.
    dental preparations, especially Mercury (Hg).                 Data have first been observed considering the pres-
    Dysfunctional problem analysis: correlates the dys-           ence of heavy metals, and subsequently analyzed in
    functional characteristics, such as pathology and             the different sample groups.
    pain, with the occurrence of heavy metals in urines,




                                                                                                                           li
    in order to highlight a possible relation between the
    two. As regards the SG, in order to carry out a more          Heavy metals analysis




                                                                      na
    significant check of the relation between the quantity
    of heavy metals and the seriousness of the symp-              The whole studied population presents, for most of
    toms, subjects with a higher total level of heavy met-        the metals which are taken into account, urine values
    als (Gr1) and metals present in dental preparations           superior to the “reference values for Italian population




                                                                    io
    (Gr1OD) have been compared with patients present-             (RV)” (27). Each subject, independently from the
    ing a minor level of total heavy metals (Gr3) and of          group, presents levels which are over the threshold
    the most frequent metals in dental preparations               for at least 4 of the 19 metals taken into account.
    (Gr3OD) (Tab.6, 7).                                           (Figs. 1-2)




                                                                 az
    To verify the reliability, the data have been crossed         Yet, the Study Group presents the absolute highest
    for metals and pathology/symptomatology, the vari-            levels, compared to the whole Control Group. The
    ous metals have been quantified in the selected               higher presence of metals in SG than in CG, in terms
    groups, and subsequently, the presence of metals in           of variance entity from RV, is well highlighted from




                                                              rn
    the different dysfunctional typologies has been also          the results obtained by the Student’s t-test, which
    evaluated (Fig. 7-16 in the results paragraph).               made the comparison possible among the variance
    Statistical analysis: the data obtained from urine            means from RV (vmRV) of all metals:




                                                           te
    analysis and those related to the pathological and                          Total metals (19): t = 0.2715;
    symptomatological aspects are not time-variant, that is,                  P (level of significancy) = 0.7876
    we do not have any data referring to any 0 time and           Another interesting result, in terms of variance entity
    subsequent phases; thus, a descriptive statistic analy-       from RV, is obtained by the internal CG group com-
    sis has been carried out, in order to synthesize the
    available data through graphic instruments (his-
                                                        In        parison, that is, between the CG1 and CG2 sub-
                                                                  groups. The analysis of the vmRV, for all the exam-
    tograms), as well as indexes (the mean of variances           ined metals and considering these two groups sepa-
    from RV) describing the most important aspects. In par-       rately, has highlighted that CG1 presents a larger
    ticular, this kind of analysis has been of both qualitative   number of heavy metals than CG2.
                                           ni
    (presence/absence of heavy metals in urines and of a          Student’s t-test has actually proved significant:
    dysfunctional symptomatology) and quantitative (level                   Comparison GC1 – GC2: t = 0,1193;
    of heavy metals) nature. For the quantitative data, “Stu-                 P (level of significancy) = 0,9057
    dent's t-test” has been applied (the difference between       Another datum that has emerged analyzing metals in
                               o

    the observed means is not significant for p<0,05).            the different samples, concerns the so-called “OD
                                                                  metals” group (10 metals), namely those heavy met-
                           izi


                                                                  als that can be found in dental alloys and in amal-
    Results                                                       gams, which are thus of specific interest for us.
                                                                  Six of these present a higher variance from the RV in
    A large quantity of data have emerged from the                the SG patients (Tab. 8), while the remaining 4, with
            Ed




    analysis and the comparisons between the various              levels over the threshold, are more frequent in the
    sample groups, consequently only the most signifi-            CG patients (Tab. 9).
                                                                  The most frequently occurring elements in SG pa-
                                                                  tients, particularly Mercury (Hg), are by far the most
    Table 6. SG subdivision according to the number of total      represented metals in dental materials. This datum
    metals.                                                       confirms and reinforce the sample division that has
    C




                                                                  been made in the research.
             Pt. N°        % of SG   Total heavy metals (19)      The Student’s t-test is also significant:
CI




    Gr1      6             12 %      > 10metals                                  OD Metals (10): t = 0.9735;
    Gr2      26            52%       5< metals ≤ 10                           P (level of significancy) = 0.3448
    Gr3      18            36%       1≤ metals ≤ 5                The results emerging from the statistic analysis and the
                                                                  descriptive analysis, which is expressed in percent-
                                                                  ages, confirm each other, thus resulting significant.
                                                                  “OD metals” are present with higher values than RV
©




    Table 7. SG subdivision according to the number of OD
                                                                  also in patients who have prosthesis and/or orthodon-
    metals.
                                                                  tic appliances (16 patients: 32% of the SG). In these
                  Pt. N°      % of SG        OD Metals (10)       patients the most occurring elements are Molybde-
                                                                  num (Mo) in 50% of the sample (8 patients), Iron (Fe)
    Gr1OD         4           8%             > 6 ODmetals         and Mercury (Hg) in 62% (10 patients), Antimony
    Gr2OD         14          28%            3< ODmetals ≤ 6      (Sb) in 69% (11 patients), and Titanium (Ti) in 100%
    Gr3OD         32          64%            1≤ ODmetals ≤ 3
                                                                  of the sample (16 patients) (Fig. 3).

    44                                                                               Annali di Stomatologia 2014; V (2): 41-51
    Heavy metals and pain in the dysfunctional patient


                                                                                                                           Figure 1. Distribution of metals increased in SG
                                                                                                                           (50 patients).


                                                                                                    1≤ metals ≤ 5




                                                                                                                                                                         li
                                                                                                    5< metals ≤ 10

                                                                                                    10< metals ≤ 15




                                                                                                        na
                                                                                                    15< metals ≤ 19




                 1≤ metals ≤ 5        5< metals ≤ 10     10< metals ≤ 15   15< metals ≤ 19




                                                                                                      io
                                                                                                                           Figure 2. Distribution of metals increased in CG




                                                                                                   az
                                                                                                                           (50 patients).


                                                                                                1≤ metals ≤ 5




                                                                                                rn
                                                                                                5< metals ≤ 10

                                                                                                10< metals ≤ 15

                                                                                                15< metals ≤ 19




                                                                                             te
                  1≤ metals ≤ 5        5< metals ≤ 10    10< metals ≤ 15 15< metals ≤ 19
                                                                                          In
    Table 8. OD Metals more in SG.                                                                            Table 9. OD Metals more in CG.

    Metal                                      SG                                  CG                         Metal                        SG                     CG
                                                                   ni
                                       N° Pt            %                   N° Pt         %                                           N° Pt     %            N° Pt %
    Zinc (Zn)                          12               24                  5             10                  Cobalt (Co)             7         14           31     62
    Molybdenum (Mo)                    19               38                  8             16                  Nickel (Ni)             12        24           35     70
                                           o

    Mercury (Hg)                       32               64                  9             18                  Indium (In)             0         0            3      6
    Titanium (Ti)                      30               60                  11            22                  Manganese (Mn)          12        24           35     70
    Antimony (Sb)                      38               76                  17            34
                                       izi



    Tin (Sn)                           5                10                  2             4
                 Ed




                                                                                                                           Figure 3. Metals with significant percentage de-
     100%
                                                                                                                      Fe
                                                                                                                           viancy in prosthetic/orthodontic patients.
     90%
                                                                                                                      Mn
     80%
                                                                                                                      Cd
     70%

     60%
                                                                                                                      Zn

                                                                                                                      Mo
    C




     50%

     40%                                                                                                              Co

     30%                                                                                                              Sn
CI




     20%                                                                                                              Ni
     10%
                                                                                                                      Hg
      0%
                                                                                                                      Sb
            Fe       Mn          Cd       Zn      Mo         Co     Sn       Ni      Hg        Sb        Ti
©




    The most interesting result with Mercury (Hg) is that                                                     Dysfunctional problem analysis
    the variance from the reference value is proportional
    to the number of amalgam fillings in the single pa-                                                       The presence of heavy metals in the different dysfunc-
    tient’s oral cavity (Fig.4); therefore, it seems that                                                     tional pathologies has been evaluated, and in order to
    there might be a direct relation between the number                                                       proof the results, the data have been crossed contrari-
    of fillings and the increased release of metal ions in                                                    wise; that is, in the different dysfunctional/symptomato-
    the oral cavity.                                                                                          logical groups, metals have been quantified. To have a

    Annali di Stomatologia 2014; V (2): 41-51                                                                                                                            45
    C. Di Paolo et al.


    complete vision and a more specific comparison of the        As regards the the IIa severe, in a total of 13 patients
    data, the different groups have been compared: dysfunc-      Gr1occurs in 83% (19 patients) and Gr1OD in 100%
    tional subjects with metal preparations in the oral cavity   (23 patients); Gr3 is present in 33% (7,59 patients),
    (SG: 50 patients, 100% of SG), the dysfunctional ones        Gr3OD in 31% (7,13 patients), CG1in 27% (6,21 pa-
    without any metal preparations in the oral cavity (CG1:      tients) and CG2 in 0% (0 patients). As regards the IIIc




                                                                                                                           li
    15 patients, 30% of the CG) and also those non-dysfunc-      severe, in a total of 7 patients Gr1 present in 33%
    tional subjects without any metal preparations in the oral   (2,31 patients), Gr1OD in 50% (3,50 patients), Gr3 in




                                                                     na
    cavity (CG2: 35 patients, 70% di CG).                        17% (1,19 patients), Gr3OD in 12% (0,84 patients),
    Articular problems: the data related to the patholo-         and CG1 and CG2 in 0% (Figs.5-6).
    gies belonging to the dysfunctional groups IIa (23 pa-       Main algic symptomatology: TMJ pain (IIIa) and
    tients: 23% of the sample) and IIIc severe (7 patients:      MM pain.




                                                                   io
    7% of the sample) have resulted significant. Crossing        TMJ pain is mainly referred to as severe/very severe:
    them with the quantitative subdivision of the metals, it     in a total of 31 patients (48% of the sample) Gr1 oc-
    has resulted that in both pathologies the most fre-          curs in 84% (26 patients), Gr1OD in 75% (23 pa-
    quent groups are Gr1 and Gr1OD.                              tients), Gr3 in 55% (17 patients), Gr3OD in 50% (15




                                                                az
                                                                          Figure 4. Hg amount in SG patients with amal-




                                                             rn
                                                                          gam fillings.




                                                          te
                                                       In
                                          ni

                                                                          Figure 5. Metals – Articular problems.
                             o
                         izi
           Ed
    C




                                                                          Figure 6. Articular problems – Metals.
CI
©




    46                                                                               Annali di Stomatologia 2014; V (2): 41-51
    Heavy metals and pain in the dysfunctional patient


    patients), CG1 in 20% (6 patients) and CG2 in 0% (0     patients), CG1 in 27% (7 patients), CG2 in 0% (0 pa-
    patients).                                              tients).
    In all the examined groups TMJ pain has been defined    Muscular pain has been defined as mild by a lower
    mild/moderate by a minor percentage: in a total of 17   percentage in all the examined groups: in a total of 8
    patients (26% of the sample) Gr1 is present in 17% (3   patients (12% of the sample) Gr1 and Gr1OD are




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    patients), Gr1OD in 25% (4 patients), Gr3 in 16% (3     present in 0% (0 patients), Gr3 in 8% (0,64 patients),
    patients), GrOD in 25% (4 patients), CG1 in 33% (6      Gr3OD in 19% (1,52 patients), CG1 in 7% (0,56 pa-




                                                                       na
    patients) and CG2 in 0% (0 patients) (Figs.7-8).        tients) and CG2 in 0% (0 patients) (Figs. 9-10).
    Muscular pain has been mainly referred to as severe:    Comorbidity: headache and cervicalgia.
    in a total of 27 patients (41% of the sample) Gr1 Is    Headache is represented mainly as severe/very se-
    present in 83% (22 patients), Gr1OD in 75% (20 pa-      vere in all the examined groups: in a total of 36 pa-




                                                                     io
    tients), Gr3 in 44% (12 patients), Gr3OD in 34% (9      tients (55% of the sample) Gr1 is present in 67% (24




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                                                                    Figure 7. Metals – TMJ pain.




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                                                                    Figure 8. TMJ pain – Metals.
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                                                                    Figure 9. Metals - MM pain.
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    Annali di Stomatologia 2014; V (2): 41-51                                                                  47
    C. Di Paolo et al.


    patients), Gr1OD in 75% (27 patients), Gr3 in 66%              the sample) Gr1 and Gr1OD are present in 50% (16
    (24 patients), Gr3OD in 69% (25 patients), CG1 in              patients), Gr3 in 67% (21 patients), Gr3OD in 63%
    33% (12 patients) and CG2 in 0% (0 patients).                  (20 patients), CG1 in 26% (8 patients) and CG2 in
    Headache has been defined as mild/moderate, instead,           0% (0 patients). Cervicalgia has been defined instead
    by a lower percentage of patients: in a total of 12 patients   as mild/moderate by a lower percentage of patients:




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    (18% of the sample) Gr1 and Gr1OD are present in 0%            in a total of 19 patients (29% patients), Gr1 is present
    (0 patients), Gr3 in 1% (0,12), Gr3OD in 6% (0,72), CG1        in 33% (6,27 patients), Gr1OD in 25% (4,75 patients),




                                                                       na
    in 54% (6,48 patients) and CG2 in 0% (Fig. 11, 12).            Gr3 in 17% (3,23 patients), Gr3OD in 15% (2, 85 pa-
    As regards Cervicalgia, this has also been defined as          tients), CG1 in 47% (8,92 patients) and CG2 in 0% (0
    severe/very severe: in a total of 32 patients (49% of          patients) (Fig. 13, 14).




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                                                                            Figure 10. MM pain – Metals.




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                                                                            Figure 11. Metals – Headache.
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                                                                            Figure 12. Headache – Metals.
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    48                                                                                Annali di Stomatologia 2014; V (2): 41-51
    Heavy metals and pain in the dysfunctional patient


                                                                        Figure 13. Metals – Cervicalgia.




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                                                                        Figure 14. Cervicalgia – Metals.




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    Discussion                                                 due to the scarcity of the sample, rather than to typol-
                                                               ogy of dysfunction.
                              o

    The above reported results agree with those studies        The SG patients with the more serious forms (IIa se-
    that underline how much environmental exposition           vere and IIIc severe) present a higher percentage of
                          izi


    factors such as air, water, and food are relevant          total heavy metals (Gr1, 6 patients: 12% of the SG),
    sources of contamination for the whole population,         and metals from dental preparations (Gr1OD, 4 pa-
    both healthy and affected by pathology (28,29). In         tients: 8% di SG). The percentage deviancy of this
    fact, the CG1(dysfunctional subjects without dental        above mentioned serious sample is significant if con-
           Ed




    preparations in the oral cavity) presents high concen-     fronted with the deviancy of patients presenting a
    trations of metals that may make the dysfunction           lower level of heavy metals, both total (Gr3, 18 pa-
    worse. Even if within the limits of this sample, this is   tients: 36% of SG) and OD metals (Gr3OD, 32 pa-
    a presumable result because there is a directly pro-       tients: 64% of SG).
    portional tendency between the concentration of met-       Inside the control group (CG1+CG2) the IIa severe
    al ions and the exacerbation of the clinical sympto-       represents the 26% (4 patients) of the CG1 (15 patients:
    C




    matology.                                                  30% of the CG) and IIIc the 0% (no patients), while in
    The obtained results, moreover, seem to coincide           the CG2 there is no pathology represented (Figs. 5-6).
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    with those researches that show how dental materi-         As regards the main algic symptomatology (TMJ
    als, especially those present in the amalgams, can         pain, MM pain) in patients belonging to the SG, it is
    release metal ions in the organism (30) (Figs. 3-4).       mainly severe or very severe, even if with different
    As regards the considered pathologies, the most            percentages according to the groups (84-83% of Gr1;
    significant data are to be found in the severe forms       75% of Gr1OD; 55-44% of Gr3; 50-34% of Gr3OD).
    (for the presence of pain), and in particular in the Re-   In CG the TMJ pain is defined mainly as mild (33% of
©




    ducible disc displacement (IIa according to the            CG), and MM pain, conversely, as severe (27% of
    RDC/TMD), and the TMJ arthrosis (IIIc according to         CG). The most interesting evidence is that, in the
    the RDC/ TMD). Insignificant, and thus not reported,       Gr1and Gr1OD groups, we find the highest percent-
    are the dysfunctional forms related to the group of the    ages of TMJ and MM pain referred to as severe/very
    Irreducible disc displacement (IIb according to the        severe (Figs. 7-10).
    RDC/TMD; 3 patients: 6 % in SG-1 patient: 2% in            As regards comorbidity (headache and cervicalgia),
    CG). The scarce validity of the data for this groups is    it also proved severe or very severe in the SG, al-


    Annali di Stomatologia 2014; V (2): 41-51                                                                       49
    C. Di Paolo et al.


    though no pivotal percentage variances are found in                  5. De Laat A. Temporomandibular Disorders as a source of oro-
    the various subgroups (67-50% of Gr1; 75-50% of                         facial pain. Acta neurol belg. 2011;101:26-31.
    Gr1OD; 66-67% of Gr3; 69-63% of Gr3OD). The pa-                      6. Molina OF, Aquilino RN, Rank R, Santos ZC, Manzutti Eid
    tients of the CG, on the contrary, report lower values                  NL, Tavares PG. Is inflammation a mechanism in arthrogenic
                                                                            TMJ Otalgia? Rev Neurocienc. 2011;19(4)632-641.
    (mild for 54-47% of the sample) (Figs. 11-14).




                                                                                                                                         li
                                                                         7. Alstergren P, Kopp S. Prostaglandin E2 in temporo-
                                                                            mandibular joint synovial fluid and its relation to pain and in-




                                                                            na
                                                                            flammatory disorders. J Oral Maxillofac Surg. 2000;58(2):180-
    Conclusions                                                             6;discussion 186-8.
                                                                         8. Alstergren P. Cytokines in temporomandibular joint arthritis.
    The obtained results seem to highlight a certain direct                 Oral Dis. 2000;6(6):331-4.
    proportionality between dysfunction and algic sympto-                9. Balkowiec-Iskra E. The role of immune system in inflammatory




                                                                          io
    matology seriousness and the increased concentra-                       pain pathophysiology. Pol Merkur Lekarski. 2010;29(174):
    tion of heavy metals in all the examined groups and                     395-9.
    subgroups.                                                          10. Haskin CL, Milam SB, Cameron IL. Pathogenesis of de-
                                                                            generative joint desease in the human temporomandibular




                                                                       az
    This data may be linked to some hypotheses found in
                                                                            joint. Crit Rev Oral Biol Med. 1995;6(3):248-277.
    the literature. Among these, we remember those by                   11. Moalem G, Tracey D. Immune and inflammatory mechanisms
    De Bont and Stegenga (1997) (3,4) or Kacena at al.                      in neuropathic pain. Brain Res Rev. 2006;51(2):240-64. Epub
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                                                                        12. Sommer C, Kress M. Recent findings on how proinflammatory
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    (6), who link it to the appearance of articular and                     tory and neuropathic hyperalgesia. Neurosci Lett. 2004;361(1-
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                                                                        13. Wang XD, Kou XX, Mao JJ, Gan YH, Zhou YH. Sustained




                                                                 te
    (2001) (5) find a correlation between the inflammation
    and the insurgence of an oxidative stress condition,                    inflammation induces degeneration of the temporomandibular
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                                                                        14. Hogan MC. Heavy metal. Encyclopedia of Earth. National
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    In particular, this research has pointed out, for the
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                                                                        15. Manzon L, Grippaudo G. Fondamenti di materiali dentari.
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    tors of the inflammation and/or of its progression.                     1999.
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    Some metals can also cause an oxidative stress in-                  17. Nordberg G, Fowler B, Nordberg M, Friberg L. Handbook on
    crease, being able to catalyze the decomposition of                     the Toxicology of Metals. Elsevier, 2008.
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                               o

                                                                            74:793-807.
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                                                                            of oxidative stress in temporomandibular disorders: a pilot
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    Annali di Stomatologia 2014; V (2): 41-51                                                                                                 51
