Yesterday, new NHANES 2009-2012 data on prevalence, extent and severity of periodontitis have gone online in the Journal of Periodontology. On first sight, authors confirm findings of the previous, 2009-2010, survey in that prevalence is much larger as previously reported. So, 46% of U.S. adults have periodontitis with almost 9% having severe disease (Eke et al. 2015). The previous report (Eke et al. 2012a) contained an unclear description of how attachment loss was measured concealing that a “signed” measure of recession was used to calculate clinical attachment loss as difference of probing pocket depth and recession (from Latin, recessus, retreat). In a letter to the Editor-in-Chief of the Journal of Dental Research, Professor Giannobile, I had raised more problems in the article when I wrote,
“Teaching in particular undergraduates about how probing parameters periodontal probing depth, attachment level, and recession are measured is quite an effort but usually straightforward. In order to avoid undue exaggeration of prevalence, extent and severity of periodontitis both in the population and in patients attending a common office and to be able to assess treatment outcomes, metric periodontal probing parameters have to be properly defined. I would therefore appreciate if authors could comment on the apparent redefinition of attachment loss in their paper. When analyzing the Figure in the paper by Eke et al. (2012a), what immediately hits the eye is that there seems to be higher prevalence of attachment loss at different thresholds (a) than of pocket depth at respective thresholds (b) in all age groups. Such a pattern may actually be a result of how attachment loss had erroneously been redefined, most probably due to convenience. Just as a trivial example, a 4 mm probing depth without recession may be associated with either 0, 1, 2, 3, or 4 mm attachment loss, but the NHANES oral health data management program would have “instantly calculated” 4 mm. Based on the new case definition using attachment loss in addition to probing depth, prevalence of all periodontitis in the adult population of 30 years and older in the U.S. has now been estimated to exceed 47%, after 35% found in NHANES III during 1988-1994. This much higher prevalence may be due to the redefinition of attachment loss, too. Moreover, as to Eke et al. (2012a), mild periodontitis has a rather low prevalence in all age groups while moderate periodontitis is widespread (Figure c). The picture was different in NHANES III when severe periodontitis occurred with lowest, moderate periodontitis with intermediate and mild periodontitis with highest prevalence, a pattern which, I suppose, applies to many other widespread chronic diseases. The strange new pattern might indeed be explained partly by the redefinition of attachment loss as well, ultimately leading to a different distribution of cases.” (Emphasis added.)
Subtracting recession from periodontal probing depth makes sense only when true recession (the free gingival margin is located apical to the cemento-enamel junction) gets a minus sign. This was circumstantially explained to me in an email by the authors forwarded to me by Professor Giannobile, who never published my original letter. Eke et al. (2012a) had actually concealed that a signed recession definition was used. In the new update of NHANES 2009-2012, calculation of clinical attachment is now correctly described, including the signed recession definition. Eke et al. (2015) may also have realized that there is no complex chronic disease where moderate severity is more prevalent than its mild form. It is rather perplexing to see that authors have now abandoned the differentiation between moderate and mild periodontitis which they call “other” periodontitis (other than severe). They give the following reason,
“These subgroups [mild and moderate periodontitis] are not truly ordinal [sic] as the label suggests because many ‘moderate’ cases had insufficient pocket depth to qualify as ‘mild’ and we have therefore combined them and used the label ‘other‘ periodontitis.”
As many readers may have noted , I had been quite concerned about how clinical attachment level (CAL) had been measured in the 2009-2010 continuous NHANES which had been reported in 2012 by Eke et al. (Note: 2011-2012 continuous NHANES has been completed and periodontal results are probably being published soon). After having adopted full-mouth, including 6 sites per tooth, recording and a different case definition, authors had reported quite dramatic higher prevalence of, in particular, moderate periodontitis in the adult population of the U.S. as compared to prevalence reported in NHANES III (Albandar et al. 1999). Another possible amendment was how CAL was calculated.
As for NHANES III, Albandar et al. (1999) had explained the procedure as follows.
The distance from the cemento-enamel junction (CEJ) to the free gingival margin (FGM) and the distance from the FGM to the bottom of the pocket/sulcus were assessed at the mesio-buccal and mid-buccal surfaces. The measurements were made in millimeters and were rounded to the lowest whole millimeter. The assessment was made by using the NIDR periodontal probe. The probing depth was defined as the FGM/sulcus measurement. The CEJ/FGM distance was given a negative sign if the gingival margin was located on the root. Attachment loss was defined as the distance from CEJ to the bottom of the pocket/sulcus and was calculated as the difference between CEJ/FGM and FGM/sulcus distances (or the sum of the 2 distances if FGM was on the root).
Interestingly, Albandar et al. (1999) do not mention recession but rather distances between well-defined landmarks. In contrast, Eke et al. (2012) describe,
All periodontal examinations were conducted in a mobile examination center (MEC) by dental hygienists registered in at least one U.S. state. Gingival recession [= the distance between the free gingival margin (FGM) and the cemento-enamel junction (CEJ)] and pocket depth (PD) (= the distance from FGM to the bottom of the sulcus or periodontal pocket) were measured at 6 sites per tooth (mesio-, mid-, and disto-buccal; mesio-, mid-, and disto-lingual) for all teeth, excluding third molars. For measurements at each site, a periodontal probe (Hu-Friedy PVP 2TM, Chicago, IL, USA) with 2-, 4-, 6-, 8-, 10-, and 12-mm graduations was positioned parallel to the long axis of the tooth at each site. Data were recorded directly into an NHANES oral health data management program that instantly calculated attachment loss (AL) as the difference between probing depth and recession. Bleeding from probing and the presence of dental furcations were not assessed. (Emphasis added.)
Note that Eke et al. (2012) mention “recession” rather than the (signed) distance CEJ/FGM.
Eke et al. later clarified in a letter to the editor of the Journal of Dental Research, Dr. William Giannobile (which was kindly provided to me via email) that the procedures were essentially identical in NHANES III and continuous 2009-2010 NHANES and had actually been adopted for decades. As Drs. Eke et al. wrote to Dr. Giannobile,
The algorithm used to calculate attachment loss (AL) in NHANES can intuitively be misunderstood because it is stated that subtraction measures of gingival recession from measures of pocket depth PD (and not added as one would expect intuitively). However, mathematically this is correct. The recession is called out as a negative number by the examiner and is subtracted from the PD i.e., PD – (-recession) = PD + recession (if the FGM is below the CEJ) which adds up to the sum of the recession plus the PD. If the FGM is above the CEJ, then it is the direct sum of the recession (which is positive) and PD. Thus in NHANES, AL is calculated from three anatomical points versus a direct measure from the CEJ to the bottom of the pocket as may be done clinically (Clinical attachment loss). There is a long history behind why NCHS has used this approach, however this is how AL has been determined for all previous NHANES including NHANES III (the dataset used by Albandar 1999), NHANES 1999-2004 and NHANES 2009 – 2010.
Note that “recession” (from Latin recessus, i.e. “retreat”) cannot reasonably be negative. At least that won’t make too much sense but easily confuses readers and scientists, both within and outside our main professional field. This is, by the way, a lengthy explanation of why a very circumstantial definition of a straightforward and intuitive distance between landmarks, one well- and the other rather ill-defined (see below), may be “mathematically correct” but completely delusive. I am afraid that recent misconceptions about what is clinical attachment loss (see, for instance, my former colleagues’ recent case-control study of periodontal disease in type 1 diabetic children) are mainly due to the confusing description by Eke et al. (2012).
Moreover, common dental recording systems including Tromsø University Dental Clinic’s and Dental Competence Center’s Opus rely on recession (i.e. real gingival retraction) and periodontal probing depths. Attachment levels can not even be recorded. Adding zero retraction to probing depth would not automatically yield attachment loss. Educating undergraduates about attachment loss and, based on that, contemporary case definitions (Page and Eke 2007) is in fact difficult if findings have to be entered into an insufficient recording system. When data are research findings, conclusions might be spurious.
As I have reported in my previous post, in the current controversy with authors of a recent update of prevalence of periodontal disease in the U.S. as observed in the 2009-2010 NHANES, the editor of Journal of Dental Research, Professor W. Giannobile, had expressed regrets that he has declined to publish either an Erratum or my letter [pdf]. According to Dr. Giannobile, authors had conceded that
“[T]he algorithm used to calculate attachment loss (AL) in NHANES can intuitively be misunderstood because it is stated that subtraction measures of gingival recession from measures of pocket depth PD (and not added as one would expect intuitively). However, mathematically this is correct. The recession is called out as a negative number by the examiner and is subtracted from the PD i.e., PD – (-recession) = PD + recession (if the FGM is below the CEJ) which adds up to the sum of the recession plus the PD. If the FGM is above the CEJ, then it is the direct sum of the recession (which is positive) and PD. Thus in NHANES, AL is calculated from three anatomical points versus a direct measure from the CEJ to the bottom of the pocket as may be done clinically (Clinical attachment loss). There is a long history behind why NCHS [National Center of Health Statistics] has used this approach, however this is how AL has been determined for all previous NHANES including NHANES III (the dataset used by Albandar 1999), NHANES 1999-2004 and NHANES 2009 – 2010.”
Honestly, I had not expected anything else. The authors actually claim that they had adopted the “long history” of how attachment loss had been determined, i.e. according to the correct albeit overly complicated approach used by Albandar et al. (1999) but, for the first time, mention “recession” rather than the distance between the cemento-enamel junction and the free gingival margin (which got a minus sign in case of exposed root surface). In my response I wrote,
“[I]f the ways how attachment loss have been determined had been identical in NHANES III and the 2009-2010 NHANES (and indeed any NHANES), one would expect either an apt quotation or a correct reference.
Note that Albandar et al. (1999) did not use the term “recession” at all in their description of what had been considered attachment loss. I find it very awkward that recession (from Latin recessus, retreat) can have a minus sign. I am afraid that future investigators outside the U.S. might refer to Eke et al. (2012) when falsely calculating attachment loss by intuitively and erroneously adding (rather than subtracting) recession and periodontal probing depth. See also the description, apparently written for lay people, of what is meant by recession and attachment loss in Dye et al. (2007) on p. 102 who compare NHANES III and 1999-2004 NHANES data:
“Recession: the presence of exposed [sic!] dental root, which is typically measured in millimeters from the free gingival margin (FGM) to the cemento-enamel junction (CEJ). The FGM is located along the top of the gum and the CEJ is the place on a tooth where the root and the tooth “crown” meet.
“Attachment loss (AL): the amount of connective tissue loss measured in millimeters (mm) from the CEJ to the sulcus base.”
I still would find a brief Corrigendum or Erratum or, say, Note regarding the paper by Eke et al. appropriate and helpful, which might state that attachment loss had been determined in an identical way as had been described by Albandar et al. (1999).
As regards my final suggestion, I am aware that case definitions by Albandar et al. (1999) did include furcation involvement which has not been assessed by Eke et al. (2012). So, direct comparison in order to conclude whether the situation has improved, is stable, or has actually deteriorated will in fact hardly be possible.” (Emphasis as such.)