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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Tooth loss is associated with increased risk of esophageal cancer: evidence from a meta-analysis with dose-response analysis</title><author><name sortKey="Chen, Qi Lin" sort="Chen, Qi Lin" uniqKey="Chen Q" first="Qi-Lin" last="Chen">Qi-Lin Chen</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Zeng, Xian Tao" sort="Zeng, Xian Tao" uniqKey="Zeng X" first="Xian-Tao" last="Zeng">Xian-Tao Zeng</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation><affiliation><nlm:aff id="a2"><institution>Center for Evidence-Based and Translational Medicine, Department of Stomatology, Zhongnan Hospital of Wuhan University</institution>, Wuhan 430071,<country>P.R. China</country></nlm:aff></affiliation></author><author><name sortKey="Luo, Zhi Xiao" sort="Luo, Zhi Xiao" uniqKey="Luo Z" first="Zhi-Xiao" last="Luo">Zhi-Xiao Luo</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Duan, Xiao Li" sort="Duan, Xiao Li" uniqKey="Duan X" first="Xiao-Li" last="Duan">Xiao-Li Duan</name><affiliation><nlm:aff id="a3"><institution>Department of Digestive Medicine, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan, 442000,<country>P.R. China</country></nlm:aff></affiliation></author><author><name sortKey="Qin, Jie" sort="Qin, Jie" uniqKey="Qin J" first="Jie" last="Qin">Jie Qin</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Leng, Wei Dong" sort="Leng, Wei Dong" uniqKey="Leng W" first="Wei-Dong" last="Leng">Wei-Dong Leng</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26742493</idno><idno type="pmc">4705514</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4705514</idno><idno type="RBID">PMC:4705514</idno><idno type="doi">10.1038/srep18900</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000829</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000829</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Tooth loss is associated with increased risk of esophageal cancer: evidence from a meta-analysis with dose-response analysis</title><author><name sortKey="Chen, Qi Lin" sort="Chen, Qi Lin" uniqKey="Chen Q" first="Qi-Lin" last="Chen">Qi-Lin Chen</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Zeng, Xian Tao" sort="Zeng, Xian Tao" uniqKey="Zeng X" first="Xian-Tao" last="Zeng">Xian-Tao Zeng</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation><affiliation><nlm:aff id="a2"><institution>Center for Evidence-Based and Translational Medicine, Department of Stomatology, Zhongnan Hospital of Wuhan University</institution>, Wuhan 430071,<country>P.R. China</country></nlm:aff></affiliation></author><author><name sortKey="Luo, Zhi Xiao" sort="Luo, Zhi Xiao" uniqKey="Luo Z" first="Zhi-Xiao" last="Luo">Zhi-Xiao Luo</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Duan, Xiao Li" sort="Duan, Xiao Li" uniqKey="Duan X" first="Xiao-Li" last="Duan">Xiao-Li Duan</name><affiliation><nlm:aff id="a3"><institution>Department of Digestive Medicine, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan, 442000,<country>P.R. China</country></nlm:aff></affiliation></author><author><name sortKey="Qin, Jie" sort="Qin, Jie" uniqKey="Qin J" first="Jie" last="Qin">Jie Qin</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Leng, Wei Dong" sort="Leng, Wei Dong" uniqKey="Leng W" first="Wei-Dong" last="Leng">Wei-Dong Leng</name><affiliation><nlm:aff id="a1"><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></nlm:aff></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Epidemiological studies have revealed the association between tooth loss and the risk of esophageal cancer (EC); however, consistent results were not obtained from different single studies. Therefore, we conducted the present meta-analysis to evaluate the association between tooth loss and EC. We conducted electronic searches of PubMed until to February 10, 2015 to identify relevant observational studies that examined the association between tooth loss and the risk of EC. Study selection and data extraction from eligible studies were independently performed by two authors. The meta-analysis was conducted using Stata 12.0 software. Finally eight eligible publications with ten studies involving 3 cohort studies, 5 case-control studies, and 1 cross-sectional study were yielded. Meta-analysis identified tooth loss increased risk of EC 1.30 times (Relative risk = 1.30, 95% confidence interval = 1.06–1.60, <italic>I</italic><sup>2</sup> = 13.5%). Dose-response analysis showed linear relationship between tooth loss and risk of EC (RR = 1.01, 95%CI = 1.00–1.03; <italic>P</italic> for non-linearity test was 0.45). Subgroup analysis proved similar results and publication bias was not detected. In conclusion, tooth loss could be considered to be a significant and dependent risk factor for EC based on the current evidence.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Adegboye, A R" uniqKey="Adegboye A">A. R. Adegboye</name></author><author><name sortKey="Twetman, S" uniqKey="Twetman S">S. Twetman</name></author><author><name sortKey="Christensen, L B" uniqKey="Christensen L">L. B. Christensen</name></author><author><name sortKey="Heitmann, B L" uniqKey="Heitmann B">B. L. Heitmann</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gerritsen, A E" uniqKey="Gerritsen A">A. E. Gerritsen</name></author><author><name sortKey="Allen, P F" uniqKey="Allen P">P. F. Allen</name></author><author><name sortKey="Witter, D J" uniqKey="Witter D">D. J. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26742493</article-id><article-id pub-id-type="pmc">4705514</article-id><article-id pub-id-type="pii">srep18900</article-id><article-id pub-id-type="doi">10.1038/srep18900</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Tooth loss is associated with increased risk of esophageal cancer: evidence from a meta-analysis with dose-response analysis</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Qi-Lin</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Zeng</surname><given-names>Xian-Tao</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a2">2</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Luo</surname><given-names>Zhi-Xiao</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Duan</surname><given-names>Xiao-Li</given-names></name><xref ref-type="aff" rid="a3">3</xref></contrib><contrib contrib-type="author"><name><surname>Qin</surname><given-names>Jie</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Leng</surname><given-names>Wei-Dong</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a1">1</xref></contrib><aff id="a1"><label>1</label><institution>Department of Stomatology, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan 442000, Hubei Province,<country>China</country></aff><aff id="a2"><label>2</label><institution>Center for Evidence-Based and Translational Medicine, Department of Stomatology, Zhongnan Hospital of Wuhan University</institution>, Wuhan 430071,<country>P.R. China</country></aff><aff id="a3"><label>3</label><institution>Department of Digestive Medicine, Taihe Hospital, Hubei University of Medicine</institution>, Shiyan, 442000,<country>P.R. China</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>lengtaihe@163.com</email></corresp><fn id="n1"><label>*</label><p>These authors contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>08</day><month>01</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>6</volume><elocation-id>18900</elocation-id><history><date date-type="received"><day>28</day><month>08</month><year>2015</year></date><date date-type="accepted"><day>18</day><month>11</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2016, Macmillan Publishers Limited</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Macmillan Publishers Limited</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>Epidemiological studies have revealed the association between tooth loss and the risk of esophageal cancer (EC); however, consistent results were not obtained from different single studies. Therefore, we conducted the present meta-analysis to evaluate the association between tooth loss and EC. We conducted electronic searches of PubMed until to February 10, 2015 to identify relevant observational studies that examined the association between tooth loss and the risk of EC. Study selection and data extraction from eligible studies were independently performed by two authors. The meta-analysis was conducted using Stata 12.0 software. Finally eight eligible publications with ten studies involving 3 cohort studies, 5 case-control studies, and 1 cross-sectional study were yielded. Meta-analysis identified tooth loss increased risk of EC 1.30 times (Relative risk = 1.30, 95% confidence interval = 1.06–1.60, <italic>I</italic><sup>2</sup> = 13.5%). Dose-response analysis showed linear relationship between tooth loss and risk of EC (RR = 1.01, 95%CI = 1.00–1.03; <italic>P</italic> for non-linearity test was 0.45). Subgroup analysis proved similar results and publication bias was not detected. In conclusion, tooth loss could be considered to be a significant and dependent risk factor for EC based on the current evidence.</p></abstract></article-meta></front><body><p>Tooth loss is known to considerably influence food choice, diet, nutrition intake, and esthetics<xref ref-type="bibr" rid="b1">1</xref>. It has also has been considered to impact oral health-related quality of life<xref ref-type="bibr" rid="b2">2</xref>, aggravate people with severe mental illnesses<xref ref-type="bibr" rid="b3">3</xref>, and increase the risk of cardiovascular disease<xref ref-type="bibr" rid="b4">4</xref><xref ref-type="bibr" rid="b5">5</xref><xref ref-type="bibr" rid="b6">6</xref> as well as head and neck cancer (HNC)<xref ref-type="bibr" rid="b7">7</xref>. Zheng <italic>et al.</italic> (1990)<xref ref-type="bibr" rid="b8">8</xref> first reported that tooth loss is a strong risk factor for oral cancer, and this association was further confirmed by Zeng <italic>et al.</italic> (2013) using meta-analysis<xref ref-type="bibr" rid="b7">7</xref>. For head and neck is adjoined to esophagus; besides, tooth loss as well as HNC and esophageal cancer (EC) share common risk factors, including age, gender, diabetes, social and geographical disparities, smoking, and alcohol consumption<xref ref-type="bibr" rid="b9">9</xref><xref ref-type="bibr" rid="b10">10</xref><xref ref-type="bibr" rid="b11">11</xref><xref ref-type="bibr" rid="b12">12</xref><xref ref-type="bibr" rid="b13">13</xref><xref ref-type="bibr" rid="b14">14</xref><xref ref-type="bibr" rid="b15">15</xref><xref ref-type="bibr" rid="b16">16</xref>. Therefore, the real relationship between tooth loss and EC need to be elucidated.</p><p>Abnet <italic>et al.</italic> (2001) reported that tooth loss increased the risk of developing esophageal squamous cell carcinoma (ESCC) in China<xref ref-type="bibr" rid="b17">17</xref>. Following this, many relevant epidemiological studies have been published; however, these studies have provided inconsistent or even contradicting results. The present study aimed to systematically review existing literature and to analyze the relationship between the tooth loss and the risk of EC using a meta-analysis. We hypothesize that tooth loss is associated with an increased risk of EC.</p><sec disp-level="1"><title>Methods</title><p>This meta-analysis was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement<xref ref-type="bibr" rid="b18">18</xref>.</p><sec disp-level="2"><title>Eligibility criteria</title><p>Cohort, case-control, and cross-sectional studies that evaluated the association between tooth loss and EC while meeting the following criteria were considered eligible for inclusion: (1) full-text articles could be obtained; (2) clear diagnostic criteria for EC and definition of tooth loss were reported; and (3) either the adjusted and/or unadjusted hazard ratios (HRs), odds ratios (ORs), or relative risks (RRs) and their corresponding 95% confidence intervals (CIs) or the numbers of events that could be used for their calculation were reported. When studies with overlapping data were eligible, we chose the one with the most comprehensive information. Two authors independently evaluated the eligibility of all the retrieved studies, and disagreements were resolved by discussion.</p></sec><sec disp-level="2"><title>Search strategy</title><p>For identifying relevant studies, we conducted electronic searches of the PubMed database until February 10, 2015 using the search terms (esophageal OR oesophageal OR gullet) AND (dentition OR “tooth loss” OR edentulous OR “lost of tooth”). Reference lists of recent reviews and the selected papers and were manually screened to identify additional relevant studies and avoid erroneous exclusions. Only publications in English were included.</p></sec><sec disp-level="2"><title>Data extraction</title><p>Two authors independently extracted the following information from each eligible study: last name of the first author; year of publication; study design; country of origin; sample size; age; pathological characteristics of EC; unadjusted or adjusted ORs, RRs, and HRs and relevant 95% CIs or standard errors (SEs); and the covariates for the adjusted point estimates.</p></sec><sec disp-level="2"><title>Data analysis</title><p>Statistical analysis was performed using STATA 12.0 software. First, we transformed ORs, RRs, or HRs and their CIs to their natural logarithms and SEs. We directly considered HR as RR<xref ref-type="bibr" rid="b7">7</xref><xref ref-type="bibr" rid="b19">19</xref> and computed the combined RRs and 95% CIs from the estimates reported in each study<xref ref-type="bibr" rid="b20">20</xref><xref ref-type="bibr" rid="b21">21</xref>. Heterogeneity was quantified using <italic>I</italic><sup>2</sup> values and chi-square test<xref ref-type="bibr" rid="b22">22</xref>; when both <italic>I</italic><sup>2</sup> ≤ 50% and <italic>p</italic> > 1.0 indicated no or acceptable heterogeneity<xref ref-type="bibr" rid="b23">23</xref>, we used the fixed-effects model; otherwise, we used the random-effects model. In addition, we performed subgroup analyses on the basis of stratified ORs, RRs, and HRs, given that these pooled may result in the overestimation of OR variance<xref ref-type="bibr" rid="b24">24</xref>. We also conducted a dose-response meta-analysis using STATA 12.0 software with restricted cubic spline function by the method of Orini<xref ref-type="bibr" rid="b25">25</xref> for those studies reported sufficient data, including RRs, serving size, and the sample size in each categories. Furthermore, we performed subgroups analyses on the basis of the study design, and type of cancer, adjustment, and definition of reference group. Publication bias was assessed by visual inspection of the funnel plots<xref ref-type="bibr" rid="b26">26</xref>.</p></sec></sec><sec disp-level="1"><title>Results</title><sec disp-level="2"><title>Study selection and characteristics</title><p>From the 155 records initially identified, 8 articles involving 3 cohort studies<xref ref-type="bibr" rid="b17">17</xref><xref ref-type="bibr" rid="b27">27</xref><xref ref-type="bibr" rid="b28">28</xref>, 5 case-control studies<xref ref-type="bibr" rid="b29">29</xref><xref ref-type="bibr" rid="b30">30</xref><xref ref-type="bibr" rid="b31">31</xref><xref ref-type="bibr" rid="b32">32</xref>, and 1 cross-sectional studies<xref ref-type="bibr" rid="b33">33</xref> were selected for the present meta-analysis. A detailed flow chart of the selection process is shown in <xref ref-type="fig" rid="f1">Fig. 1</xref>.</p><p>Among the selected studies, the study of Guha <italic>et al.</italic><xref ref-type="bibr" rid="b31">31</xref> involved 2 multicentric case-control studies from central Europe (including Romania, Poland, and Russia) and Latin America (including Cuba, Argentina, and Brazil), while the other 8 were single center studies. All the cases under study were confirmed to have EC through histological, pathological or cytological means, and 6 articles of 7 studies were ESCC<xref ref-type="bibr" rid="b17">17</xref><xref ref-type="bibr" rid="b27">27</xref><xref ref-type="bibr" rid="b29">29</xref><xref ref-type="bibr" rid="b31">31</xref><xref ref-type="bibr" rid="b32">32</xref><xref ref-type="bibr" rid="b33">33</xref>. All the studies clearly defined the reference group of on the basis of tooth loss, with the major characteristics presented in <xref ref-type="table" rid="t1">Table 1</xref>. All the studies reported adjusted point estimates and 95% CIs. The adjusted covariates are shown in <xref ref-type="table" rid="t2">Table 2</xref>.</p></sec><sec disp-level="2"><title>Tooth loss and risk of EC</title><p>Among the eight included studies, two showed a significantly positive association between tooth loss and the risk of EC<xref ref-type="bibr" rid="b29">29</xref><xref ref-type="bibr" rid="b30">30</xref>, while the other six were negative<xref ref-type="bibr" rid="b17">17</xref><xref ref-type="bibr" rid="b27">27</xref><xref ref-type="bibr" rid="b28">28</xref><xref ref-type="bibr" rid="b31">31</xref><xref ref-type="bibr" rid="b32">32</xref><xref ref-type="bibr" rid="b33">33</xref>. No substantial heterogeneity among these trials was observed (<italic>I</italic><sup>2</sup> = 13.5%, <italic>p</italic> = 0.32), and the overall result based on the fixed effect model showed that tooth loss increased risk of EC by 1.30 times (RR = 1.30, 95%CI = 1.06–1.60; <xref ref-type="fig" rid="f2">Fig. 2</xref>).</p><p>Five studies provided sufficient data of dose-response relationship. Our dose-repose meta-analysis showed an increased risk of EC corresponding to every 1 tooth loss increment (RR = 1.01, 95%CI = 1.00–1.03). No evidence of nonlinear relationship was detected (P = 0.45; <xref ref-type="fig" rid="f3">Fig. 3</xref>).</p><p><xref ref-type="table" rid="t3">Table 3</xref> shows the results of subgroup analyses. The results of all subgroup analyses showed significantly increased risk in case-control studies and in adjustments for smoking and/or alcohol.</p></sec><sec disp-level="2"><title>Publication bias</title><p>Visual inspection of the funnel plot did not identify any substantial asymmetry (<xref ref-type="fig" rid="f4">Fig. 4</xref>), which indicated no publication bias existed.</p></sec></sec><sec disp-level="1"><title>Discussion</title><p>The present meta-analysis found evidence of an association between tooth loss and the risk of developing EC, with the loss of tooth significantly increasing the risk by 30%. And the relationship between tooth loss and the risk of developing EC is linearly dependent. Subgroup analyses revealed similar results of pooled estimations, and publication bias was not observed. In fact, this significant association could be explained. Periodontal disease is a chronic inflammatory disease, which contributing to constant low-grade systemic inflammation with elevated levels of circulating inflammatory markers<xref ref-type="bibr" rid="b4">4</xref><xref ref-type="bibr" rid="b34">34</xref> and is associated with HNC<xref ref-type="bibr" rid="b35">35</xref> and EC<xref ref-type="bibr" rid="b36">36</xref><xref ref-type="bibr" rid="b37">37</xref>. Periodontal disease is the major cause of tooth loss<xref ref-type="bibr" rid="b38">38</xref><xref ref-type="bibr" rid="b39">39</xref>, and tooth loss is also a maker of systemic inflammation<xref ref-type="bibr" rid="b40">40</xref><xref ref-type="bibr" rid="b41">41</xref>. The link between inflammation and cancer has long been recognized<xref ref-type="bibr" rid="b42">42</xref><xref ref-type="bibr" rid="b43">43</xref><xref ref-type="bibr" rid="b44">44</xref><xref ref-type="bibr" rid="b45">45</xref>, and it is likely that the progression of periodontal disease to tooth loss also represents a progression in the breakdown of normal cell-cycle control and potential carcinogenesis. In addition, the progression of tooth loss destroys the normal periodontal tissue, allowing oral microorganisms to accumulate deep into the oral tissue, thereby facilitating their growth. Oral microorganisms produce greater amounts of nitrosamine<xref ref-type="bibr" rid="b46">46</xref>, which is significantly associated with the development of cancer<xref ref-type="bibr" rid="b47">47</xref><xref ref-type="bibr" rid="b48">48</xref>. It is not difficult to envisage that during normal physiological behavior such as swallowing and drinking, oral microorganisms as well as the produced nitrosamine are passed into the esophagus from the oral cavity along with food and drinks; therefore, an association between tooth loss and EC seems plausible.</p><p>Subgroup analyses provided varied results of cross-sectional study design, which could be partly due to the smaller number of included studies or the limitations of this design; however, the pooled results from case-control studies and cohort studies presented a significantly increased risk of EC associated with tooth loss (<xref ref-type="table" rid="t3">Table 3</xref>). On the other hand, according to the Hill’s criteria, which are widely accepted for determining causality<xref ref-type="bibr" rid="b49">49</xref>, our meta-analysis indicates that tooth loss is a marker rather than a causal factor for EC. In our meta-analysis, all included studies did not show consistency in results, and pooled RRs only showed a weak association. In addition, only 3 cohort studies among the 10 included studies involved to temporality, although their pooled result showed a significant association. Furthermore, there is no evidence whether control of tooth loss can prevent EC up to now; therefore, the specificity of the association cannot be evaluated. Moreover, there is lack of experimental research. In summary, these factors suggest that that tooth loss is a marker rather than a causal factor for EC.</p><p>The heterogeneity was none to mild among the studies examining the association between tooth loss and the risk of EC<xref ref-type="bibr" rid="b23">23</xref>. This mild heterogeneity can be attributed to the differences in the characteristics of different populations, definitions of the reference and tooth loss group(s), and adjustment for confounding factors. Our subgroup analyses provide evidence that the study design, definition of the reference group, reported effect size, pathological type, and adjustment of origin was not the source of the heterogeneity (<xref ref-type="table" rid="t3">Table 3</xref>). Hence, the mild heterogeneity might be the inherent shortage of meta-analysis or due to the statistic heterogeneity.</p><p>Our meta-analysis also has some strengths and implications. To the best of our knowledge, this study is the first meta-analysis on this topic. We have searched relevant published studies via electronic and manual searching and collected all published studies that met the inclusion criteria; no publication bias has been detected. In addition, all included studies provided adjusted effect sizes. Nine studies have adjusted for smoking, while 7 have simultaneously adjusted for smoking and alcohol (<xref ref-type="table" rid="t2">Table 2</xref>). For smoking and alcohol are the well accepted risk factor of EC<xref ref-type="bibr" rid="b9">9</xref><xref ref-type="bibr" rid="b10">10</xref><xref ref-type="bibr" rid="b11">11</xref><xref ref-type="bibr" rid="b12">12</xref><xref ref-type="bibr" rid="b13">13</xref><xref ref-type="bibr" rid="b14">14</xref><xref ref-type="bibr" rid="b15">15</xref><xref ref-type="bibr" rid="b16">16</xref>, we conducted subgroup analysis to investigate the smoking adjusted studies and both smoking and alcohol adjusted studies, the results were both significantly and similar. Thereby ensuring the accuracy of the results obtained and indicating that tooth loss is independent of the conventional risk factors for EC. Furthermore, accumulating evidence and the large sample size of included studies provide the statistical power to present precise and reliable risk estimates relative to a single study. The results of the included studies are not consistent, and subgroup analysis revealed that the sample size could influence the result. Moreover, we could not identify a causal relationship between tooth loss and the risk of EC; the actions, such as toothbrushing<xref ref-type="bibr" rid="b32">32</xref><xref ref-type="bibr" rid="b50">50</xref> are suggested to prevent tooth loss and this may decrease the risk of developing EC. Relevant animal studies and interventional studies are necessary to further explore the association between tooth loss and EC. Finally, people who cessation smoking, mild drinking, daily use of dental floss, and seeks periodontal therapy are all important ways of countering the increased risk of EC in these subjects.</p><p>Despite these strengths, several limitations should be acknowledged in our meta-analysis. First, the definition of the reference group and tooth loss used varied among studies. Nowadays, no international unification index for evaluating tooth loss in relevant studies is available, which could result in heterogeneity and increase the difficulty of performing meta-analysis, even resulting in failure to meet the criteria for meta-analysis. Second, substantial heterogeneity was observed among studies, although it was mild and very commonly found in meta-analysis of observational studies and is understandable, which cannot be ignored. We have investigated heterogeneity using subgroup analyses; however, the real source(s) of heterogeneity could not be identified. Third, subgroup analyses revealed that the results are significantly inconsistent with limited statistical power owing to a relatively small number of included studies. We used Hill’s criteria to argue causality and have discussed how the results could be influenced by the sample size; greater numbers of relevant studies addressing this topic are required for enlarging the sample size. Furthermore, while almost all included studies have adjusted for smoking and alcohol consumption, other unmeasured factors, such as diabetes, gastroesophageal reflux, and socioeconomic factors may confound the interpretation of an association between tooth loss and EC and potentially introduce bias. Only a few included studies have adjusted for these factors (<xref ref-type="table" rid="t2">Table 2</xref>). Fourth, although no evidence of publication bias was observed, the statistical power of our study is limited by a relatively small number of included studies; thus, it is difficult to be certain that there is no publication bias. These limitations of the present meta-analysis may affect the accuracy of our results. Finally, for lacking of relevant assessment tool of cross-sectional study, we could not assess the risk of bias of included studies<xref ref-type="bibr" rid="b51">51</xref>.</p><p>In summary, the present meta-analysis indicates that tooth loss is probably a significant and dependent risk factor for EC, suggesting that people who have lost teeth should pay attention to the symptoms and avoid other classical risk factors for EC. Moreover, according to the Hill’s criteria for causal inference, tooth loss is a marker rather than causality for EC.</p></sec><sec disp-level="1"><title>Additional Information</title><p><bold>How to cite this article</bold>: Chen, Q.-L. <italic>et al.</italic> Tooth loss is associated with increased risk of esophageal cancer: evidence from a meta-analysis with dose-response analysis. <italic>Sci. Rep.</italic><bold>6</bold>, 18900; doi: 10.1038/srep18900 (2016).</p></sec></body><back><ack><p>This research was supported (in part) by the Nature Science Foundation of Hubei Province (2012FFB03902) and the Foundation of Evidence-based Medicine Nursery Fund of Taihe Hospital (EBM2014010), without commercial or not-for-profit sectors. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No additional external funding received for this study.</p></ack><ref-list><ref id="b1"><mixed-citation publication-type="journal"><name><surname>Adegboye</surname><given-names>A. R.</given-names></name>, <name><surname>Twetman</surname><given-names>S.</given-names></name>, <name><surname>Christensen</surname><given-names>L. B.</given-names></name> & <name><surname>Heitmann</surname><given-names>B. 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Z.X.L. and X.L.D. searched studies and collected data. J.Q. and W.D.L. analysed and explained the data. Q.L.C. and X.T.Z. drafted the manuscript. Z.X.L. and W.D.L. reviewed the manuscript. All authors read and approved the final manuscript.</p></fn></fn-group></back><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Flow chart from identification of eligible studies to final inclusion.</title><p>EC, esophageal cancer.</p></caption><graphic xlink:href="srep18900-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Forest plot of tooth loss and risk of esophageal cancer in overall population.</title><p>Guha CE 2007, the study was conducted in Europe; Guha LA 2007, the study was conducted in Latin-America.</p></caption><graphic xlink:href="srep18900-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>Dose-response analysis of every 1 tooth loss increment and risk of esophageal cancer.</title><p>The black solid line and the black long dashed line represent the estimated RRs and corresponding 95% CIs for the non-linearity. The black short dashed line represents the estimated RRs for the linearity.</p></caption><graphic xlink:href="srep18900-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>Funnel plot with pseudo-95% CIs of results of 5 studies based on the result of overall population.</title></caption><graphic xlink:href="srep18900-f4"></graphic></fig><table-wrap position="float" id="t1"><label>Table 1</label><caption><title>Characteristics of included studies in the meta-analysis.</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50">References</th><th align="center" valign="top" charoff="50">Country</th><th align="center" valign="top" charoff="50">Study design</th><th align="center" valign="top" charoff="50">Sample sizes</th><th align="center" valign="top" charoff="50">Age (yrs)</th><th align="center" valign="top" charoff="50">Outcomes</th><th align="center" valign="top" charoff="50">Definition of reference group</th><th align="center" valign="top" charoff="50">Estimation (95%CI) (Highest vs. lowest)</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Abnet 2001</td><td align="center" valign="top" charoff="50">China</td><td align="center" valign="top" charoff="50">Cohort</td><td align="center" valign="top" charoff="50">28868</td><td align="center" valign="top" charoff="50">57(12)*</td><td align="center" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">None lost tooth</td><td align="center" valign="top" charoff="50">0.90 (0.49–1.70)</td></tr><tr><td align="left" valign="top" charoff="50">Abnet 2005</td><td align="center" valign="top" charoff="50">Finland</td><td align="center" valign="top" charoff="50">Cohort</td><td align="center" valign="top" charoff="50">29124</td><td align="center" valign="top" charoff="50">57.2 ± 5.1<sup>#</sup></td><td align="center" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">Lost ≤ 10 teeth</td><td align="center" valign="top" charoff="50">0.73 (0.35–1.55)</td></tr><tr><td align="left" valign="top" charoff="50">Dye 2007</td><td align="center" valign="top" charoff="50">China</td><td align="center" valign="top" charoff="50">CS</td><td align="center" valign="top" charoff="50">579</td><td align="center" valign="top" charoff="50">40–67</td><td align="center" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">Lost < 4 teeth</td><td align="center" valign="top" charoff="50">1.45 (0.76–2.76)</td></tr><tr><td align="left" valign="top" charoff="50">Guha 2007</td><td align="center" valign="top" charoff="50">Latin America</td><td align="center" valign="top" charoff="50">CC</td><td align="center" valign="top" charoff="50">173/1805</td><td align="center" valign="top" charoff="50">any age</td><td align="center" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">Lost ≤ 5 teeth</td><td align="center" valign="top" charoff="50">1.07 (0.41–2.77)</td></tr><tr><td align="left" valign="top" charoff="50">Guha 2007</td><td align="center" valign="top" charoff="50">Central Europe</td><td align="center" valign="top" charoff="50">CC</td><td align="center" valign="top" charoff="50">132/928</td><td align="center" valign="top" charoff="50">any age</td><td align="center" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">Lost ≤ 5 teeth</td><td align="center" valign="top" charoff="50">1.80 (1.80–4.07)</td></tr><tr><td align="left" valign="top" charoff="50">Michaud 2008</td><td align="center" valign="top" charoff="50">USA (White, Asian, Black)</td><td align="center" valign="top" charoff="50">Cohort</td><td align="center" valign="top" charoff="50">48375</td><td align="center" valign="top" charoff="50">40–75</td><td align="center" valign="top" charoff="50">EC</td><td align="center" valign="top" charoff="50">Lost ≤ 8 teeth</td><td align="center" valign="top" charoff="50">1.34 (0.78–2.30)</td></tr><tr><td align="left" valign="top" charoff="50">Abnet 2008</td><td align="center" valign="top" charoff="50">Iran</td><td align="center" valign="top" charoff="50">CC</td><td align="center" valign="top" charoff="50">283/560</td><td align="center" valign="top" charoff="50">65(56–73)/65(57–72)*</td><td align="center" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">Lost ≤ 12 teeth</td><td align="center" valign="top" charoff="50">1.79 (1.03–3.13)</td></tr><tr><td align="left" valign="top" charoff="50">Hiraki 2008</td><td align="center" valign="top" charoff="50">Japan</td><td align="center" valign="top" charoff="50">CC</td><td align="center" valign="top" charoff="50">354/708</td><td align="center" valign="top" charoff="50">20–79</td><td align="center" valign="top" charoff="50">EC</td><td align="center" valign="top" charoff="50">Lost ≤ 11 teeth</td><td align="center" valign="top" charoff="50">2.36 (1.17–4.75)</td></tr><tr><td align="left" valign="top" charoff="50">Dar 2013</td><td align="center" valign="top" charoff="50">India</td><td align="center" valign="top" charoff="50">CC</td><td align="center" valign="top" charoff="50">703/1664</td><td align="center" valign="top" charoff="50">61.6 ± 11.1/59.8 ± 11.1<sup>#</sup></td><td align="center" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">None lost tooth</td><td align="center" valign="top" charoff="50">1.08 (0.68–1.69)</td></tr></tbody></table><table-wrap-foot><fn id="t1-fn1"><p>CS, cross-sectional; CC, case-control; EC, esophageal cancer; ESCC, esophageal squamous cell carcinoma;<sup>*</sup>, median (IQR);<sup>#</sup>, mean ± standard deviation.</p></fn></table-wrap-foot></table-wrap><table-wrap position="float" id="t2"><label>Table 2</label><caption><title>Adjustments in studies included in the meta-analysis</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="left"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50">References</th><th align="left" valign="top" charoff="50">Adjustment</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Abnet 2001</td><td align="left" valign="top" charoff="50">age, gender, smoking, and alcohol</td></tr><tr><td align="left" valign="top" charoff="50">Abnet 2005</td><td align="left" valign="top" charoff="50">age and education</td></tr><tr><td align="left" valign="top" charoff="50">Dye 2007</td><td align="left" valign="top" charoff="50">age, gender, village, education, smoking</td></tr><tr><td align="left" valign="top" charoff="50">Guha 2007</td><td align="left" valign="top" charoff="50">age, gender, country/center, education, smoking, alcohol, and all other oral health variables</td></tr><tr><td align="left" valign="top" charoff="50">Abnet 2008</td><td align="left" valign="top" charoff="50">age, gender, place of residence, ethnicity, alcohol, smoking, opium, or both, education, number of appliances, and fruit and vegetable intake</td></tr><tr><td align="left" valign="top" charoff="50">Hiraki 2008</td><td align="left" valign="top" charoff="50">age, gender, tobacco, alcohol, vegetable and fruit intake, body mass index, and regular exercise</td></tr><tr><td align="left" valign="top" charoff="50">Michaud 2008</td><td align="left" valign="top" charoff="50">age, race, physical activity, history of diabetes, alcohol, body-mass index, geographical location, height, calcium intake, total calorific intake, red-meat intake, fruit and vegetable intake, vitamin D score, and smoking</td></tr><tr><td align="left" valign="top" charoff="50">Dar 2013</td><td align="left" valign="top" charoff="50">age, ethnicity, residence, education, wealth score, fruit and vegetable intake, bidi smoking, gutka chewing, alcohol consumption and cumulative use of hookah, cigarette, and nass</td></tr></tbody></table></table-wrap><table-wrap position="float" id="t3"><label>Table 3</label><caption><title>Results of subgroups analyses of pooled RRs and 95% CIs.</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col></colgroup><thead valign="bottom"><tr><th rowspan="2" align="left" valign="top" charoff="50">Subgroups</th><th rowspan="2" align="center" valign="top" charoff="50">No. of studies</th><th colspan="2" align="center" valign="top" charoff="50">Heterogeneity</th><th rowspan="2" align="center" valign="top" charoff="50">Effect model</th><th colspan="2" align="center" valign="top" charoff="50">Meta-analysis</th></tr><tr><th align="center" valign="top" charoff="50"><italic>I</italic><sup>2</sup>(%)</th><th align="center" valign="top" charoff="50"><italic>p</italic><sup><italic>h</italic></sup></th><th align="center" valign="top" charoff="50">RR (95%CI)</th><th align="center" valign="top" charoff="50"><italic>p</italic></th></tr></thead><tbody valign="top"><tr><td colspan="7" align="left" valign="top" charoff="50">Study design</td></tr><tr><td align="left" valign="top" charoff="50">Cohort</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0.39</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.02 (0.71–1.46)</td><td align="center" valign="top" charoff="50">0.91</td></tr><tr><td align="left" valign="top" charoff="50">Case-control</td><td align="center" valign="top" charoff="50">5</td><td align="center" valign="top" charoff="50">14.2</td><td align="center" valign="top" charoff="50">0.32</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.48 (1.12–1.96)</td><td align="center" valign="top" charoff="50"><0.01</td></tr><tr><td align="left" valign="top" charoff="50">Cross-sectional</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">NA</td><td align="center" valign="top" charoff="50">NA</td><td align="center" valign="top" charoff="50">NA</td><td align="center" valign="top" charoff="50">1.45 (0.76–2.76)</td><td align="center" valign="top" charoff="50">0.26</td></tr><tr><td colspan="7" align="left" valign="top" charoff="50">Outcomes</td></tr><tr><td align="left" valign="top" charoff="50">ESCC</td><td align="center" valign="top" charoff="50">7</td><td align="center" valign="top" charoff="50">1.2</td><td align="center" valign="top" charoff="50">0.42</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.21 (0.95–1.53)</td><td align="center" valign="top" charoff="50">0.13</td></tr><tr><td align="left" valign="top" charoff="50">Mixed</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">36.4</td><td align="center" valign="top" charoff="50">0.21</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.66 (1.08–2.54)</td><td align="center" valign="top" charoff="50">0.02</td></tr><tr><td colspan="7" align="left" valign="top" charoff="50">Definition of reference group</td></tr><tr><td align="left" valign="top" charoff="50">None lost tooth</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0.64</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.01 (0.70–1.46)</td><td align="center" valign="top" charoff="50">0.94</td></tr><tr><td align="left" valign="top" charoff="50">No. of lost tooth</td><td align="center" valign="top" charoff="50">7</td><td align="center" valign="top" charoff="50">6.4</td><td align="center" valign="top" charoff="50">0.38</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.46 (1.14–1.89)</td><td align="center" valign="top" charoff="50"><0.01</td></tr><tr><td colspan="7" align="left" valign="top" charoff="50">Effect estimation</td></tr><tr><td align="left" valign="top" charoff="50">Relative risk</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">NA</td><td align="center" valign="top" charoff="50">NA</td><td align="center" valign="top" charoff="50">NA</td><td align="center" valign="top" charoff="50">0.90 (0.48–1.68)</td><td align="center" valign="top" charoff="50">0.74</td></tr><tr><td align="left" valign="top" charoff="50">Hazard ratio</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">40.3</td><td align="center" valign="top" charoff="50">0.20</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.09 (0.70–1.68)</td><td align="center" valign="top" charoff="50">0.71</td></tr><tr><td align="left" valign="top" charoff="50">Odds ratio</td><td align="center" valign="top" charoff="50">6</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0.46</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.47 (1.14–1.91)</td><td align="center" valign="top" charoff="50"><0.01</td></tr><tr><td colspan="7" align="left" valign="top" charoff="50">Adjustment</td></tr><tr><td align="left" valign="top" charoff="50">Smoking</td><td align="center" valign="top" charoff="50">8</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0.46</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.37 (1.10–1.70)</td><td align="center" valign="top" charoff="50"><0.01</td></tr><tr><td align="left" valign="top" charoff="50">Smoking and alcohol</td><td align="center" valign="top" charoff="50">7</td><td align="center" valign="top" charoff="50">10.4</td><td align="center" valign="top" charoff="50">0.35</td><td align="center" valign="top" charoff="50">Fixed</td><td align="center" valign="top" charoff="50">1.36 (1.08–1.71)</td><td align="center" valign="top" charoff="50">0.01</td></tr></tbody></table><table-wrap-foot><fn id="t3-fn1"><p>No., number; ESCC, esophageal squamous cell carcinoma; RR, relative risk; CI, confidence interval.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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