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.
So far so bad. A recent study by Corraini et al. (2013) had addressed the reliability of “direct and indirect attachment level measurements”. The authors refer to an old paper by Griffiths et al. (1988) who had suggested a “direct” attachment level measurement after having pointed to the possibility of additional measurement error when measuring the attachment level “indirectly”, i.e. by subtracting the distance between the cement-enamel junction and the free gingival margin (within the periodontal pocket) from the periodontal probing depth.
Most commonly, the attachment level is assessed by probing to the bottom of the sulcus or pocket and recording first the periodontal probing depth, i.e. as described above, the distance between the free gingival margin and the bottom of the sulcus or pocket. If the CEJ is visible, the attachment level is then the distance between the bottom of the sulcus/pocket and the CEJ. Note that this is a direct measurement of the attachment level since the probe is not withdrawn. There is no need for an indirect measurement composed of two separate measurements of probing depth and recession . If the CEJ is not visible (i.e. hidden within the pocket), the CEJ has to be identified within the pocket with the tip of the probe. For that purpose, a second pass of the probe is made to measure the distance between the CEJ and the free gingival margin, and the amount subtracted from the probing depth to yield the attachment level, an indirect measurement. Consequently, both direct and indirect measurements, according to Griffiths et al. (1988), are most commonly done depending on the clinical situation.
By employing an example when the pocket depth was 2.4 mm and the clinical attachment loss 0.8 mm, Griffiths et al. (1988) explain (see original sketch below),
In order to avoid this [compound measurement] error the current method recommended […] is as follows.
(1) Measure [the distance of the] GM [gingival margin] to the base of the crevice. This is actually 2.4 mm and will be recorded as 2.0 mm.
(2) Observe, to the nearest mm, the amount of the probe withdrawn from the pocket until the CEJ is detected. This is actually 0.8 mm and will be recorded as 1.0 mm attachment level.
This gives a direct measurement rather than one derived from a computation.
Unfortunately, it is hardly possible to “observe the amount of the probe withdrawn from the pocket until the CEJ is detected.”
Corraini et al. (2013) describe the “direct” measurements in a slightly different way. Among their mentioned 5 passes (for recording supragingival plaque and calculus, probing depth and bleeding on probing, CAL, signed distance between CEJ and the gingival margin, i.e. gingival recession, but assigning, in contrast to Eke et al., a positive sign if the CEJ was located coronal to the gingival margin; and subgingival calculus), direct CAL measurement (CALDIR ) was number 3.
CALDIR was measured, as the distance from the cement-enamel junction (CEJ) to the bottom of the clinical pocket. When the FGM [free gingival margin] was located above the CEJ, that is, covering it, the periodontal probe tip was run along the tooth crown in apical direction until the CEJ was felt. At this point, a mental note was made of the position of the FGM on the probe, and the additional probing movement to the bottom of the clinical pocket, that is, the “slide” movement from the bottom of the clinical pocket to the identified CEJ position was subsequently recorded in mm, withdrawing the periodontal probe only once (Griffith et al. 1988). If the probe tip did not reach the CEJ, a CALDIR recording of 0 mm was made. When the identification of the CEJ was not possible, for example, due to the presence of a large filling or a crown, the CEJ position was defined by its most probable location using the neighbouring teeth as guidance.
The first remark about a “mental note” when inserting the probe up to the CEJ may be reasonable since this is after all the only way to assess the position of a (subgingival) CEJ in relation to the gingival margin. The second note (about attachment loss if the CEJ is destroyed) points to the common amount of guessing in the whole procedure which is, for instance, more notorious for measurements of “horizontal attachment loss” in furcations of multi-rooted where a “measurement” is suggested from an imaginary line tangent to the prominences of respective roots.
As expected, Corraini et al. (2013) calculated indirect measurement of clinical attachment loss (CALINDIR) from periodontal probing depth and (signed) gingival recession, thus intentionally introducing possible additional measurement error. All measurements were repeated about one week later.
From an analytical point of view, in order to publish observed differences in the reliabilities of direct and indirect clinical attachment level measurements, this procedure may intuitively make sense. I am afraid, however, that only nonclinicians would measure attachment loss in the way described. As mentioned above, for practical reasons and thereby intentionally reducing erroneous measurements, direct measurements are generally done in case of a visible CEJ coronal to the gingival margin (i.e. true recession). On the other hand, identification of the position of subgingival CEJ requires a different approach including a decidely indirect measurement. In that case, the probe has to be slightly tilted to tactilely note the utterly exiguous step which signals presence of CEJ. It may even be necessary to move the probe a bit (by parts of a millimeter) back and forth to confirm that step. So, claiming a single probing pass and a “mental note” when surpassing the CEJ suffices contradicts common practice of clinical assessment of periodontal disease and in fact introduces more measurement error than the procedure described above .
A final word as regards multilevel modeling of measurement differences >=1 mm of repeat probing. In a Bland-Altman plot in Fig. 2 one can identify one site where the difference between test and retest CALDIR was 10 mm while the mean of test and retest was 7 mm. That would translate to 2 mm and 12 mm at either test or retest. More sites with huge discrepancies between test and retest can be identified when direct CAL measurements had been done which apparently did not occur (at least to that extent) when indirect measurements had been made. It would have been important to have a closer look at these extremes first (e.g., 2 and 12 mm), try to identify possible reasons and possibly exclude them as outliers before deciding that this is a “measurement error of >=1 mm” and enter the site in a logistic regression analysis which identified certain local, tooth-related covariates and exactly one subject-related explanatory variable. Authors report that exploration of further sources of error would be prudent, and periodontal probing depth itself should have been considered in the models as well. And then, variance partition coefficients for various clinical conditions would have been helpful.
Based on the assumption of no real change of clinical attachment level during the observation period and adopting formulas suggested by Gunsolley and Best (1988), Corraini et al. claim that CALDIR was slightly superior as regards reliability. Well, their data set may contain much more mysteries to discover than primarily expected.
 My original posting on this blog about “How to Measure Attachment Loss” has been accessed more than 5000 times since January 2013. Although it was about my concerns regarding the paper by Eke et al. (2012) on 2009-2010 continuous NHANES periodontal data, I suppose that the main reason to google the respective question is wide-spread confusion about the procedures.
 If the main interest lies in recession, for instance when surgical root coverage is planned, a direct measurement of recession would make more sense, of course. So, different approaches of assessing periodontal probing parameters may depend on the clinician’s main focus.
 It would have been most interesting to learn in how many cases Dr. Corraini had actually applied a “plan B” strategy, i.e. guessing, from the CEJ of neighboring teeth, as CEJ could not be identified within the pocket. Unfortunately, that information is missing in her paper.
7 November 2014 @ 2:26 pm.
Last modified November 7, 2014.