The Literature That Shaped Modern Periodontology (I)

On the occasion of the celebration of AAP’s 100th anniversary this year, a reading list of highly cited and otherwise classic papers has been assembled by the editor-in-chief of the Journal of Periodontology, Dr. Kenneth S. Kornman, and AAP’s Drs. Paul B. Robertson and Ray C. Williams [1]. Authors admit that there are undoubtedly some omissions. They offer possible reasons,

For example, some important papers in the early years of periodontology may not have been highly cited because there were many fewer papers published at that time and therefore fewer opportunities to cite the paper. Similarly, some papers may have influenced clinical management of patients but did not lead to additional published work that might cite the earlier findings.

While the papers are listed within eleven themes, or unifying principles, each theme, it is promised, will be the basis for a commentary to be published during the year 2014 in the Journal of Periodontology.

I had a brief look at the extensive list and want to share with readers of my blog some ideas (and obviously missing papers) which came instantly to my mind.

Theme I. Bacteria play a critical role in the pathogenesis of periodontal disease

It appears that two groups of scientists dominate the list of highly cited papers, groups in which Jørgen Slots (6 out of 20 papers, and an additional 2 out of 4 “consensus papers of importance”) and the late Sigmund S. Socransky (9 papers plus 1) were principal investigators (the two did not collaborate). Both are known to have or have had a strong bias toward specific bacteria, or groups of bacteria, being involved in the pathogenesis of periodontitis or certain forms thereof. Advances in the microbiology of periodontal diseases definitely accelerated after Sig Socransky had published a not-so-often quoted paper in which he had tried to mitigate Robert Koch’s postulates, which were formulated almost a century earlier in 1884 and which ultimately proved Mycobacterium tuberculosis as cause of tuberculosis. Socransky’s paper on “Criteria for the infectious agents in dental caries and periodontal disease” [2] had been quoted, according to Google Scholar, just 94 times (as accessed on 22 Jan 2014), but had nevertheless an immense impact on how allegedly pivotal clinical studies had been designed in the 1980s and 1990s in order to “prove” that certain species or groups of species were involved in the etiology of both oral diseases.

Socransky (1979) mentions four criteria for the determination of an oral pathogen when he intentionally deviates from Koch’s: association with disease, the effect of elimination of the organism, the host response, and animal pathogenicity. This has sparked later dozens of studies by his group and hundreds all over the world which used thereby suggested study designs. Certainly, they ultimately led to a deeper understanding of the highly complex human oral microbiome. And in turn, the importance of certain periodontal pathogens  had to be put into relation.

Socransky (1979) does entertain, in his article, Koch’s postulates and supposes a need for their modification when it comes to dental disease. But he does not bother to mention a previous giant in epidemiology and statistics, Sir Austin Bradford Hill, who had outlined criteria for causality in complex diseases in 1965 [3]. (As fact of the matter, we learned only later that periodontitis definitely belongs to the host of complex diseases.) Major Bradford-Hill-criteria are temporality in longitudinal observational studies, i.e., the effect has to occur after the cause (and if there is an expected delay between the cause and expected effect, then the effect must occur after that delay); and strength of the association when strictly considering temporality; something which has not really penetrated throughout in the dental profession where many still consider associations in cross-sectional studies as indicative for causality. Temporality has long been disregarded (after a short period in the 1980s when researchers attempted to identify “active” disease at the site level), and few currently available longitudinal studies indicating in particular a highly leukotoxic clone of Aggregatibacter actinomycetemcomitans as causal have been conducted only during the last, say, one or two decades and mainly in Africa. Hujoel et al. (2013) [4] have recently done a systematic review and meta-analysis which clearly indicates that no other bacterium has been identified causal by applying the required epidemiological standards.

It is noteworthy that a couple of highly influential papers by not-so-much biased researchers in microbiology, some of which were also highly cited, did not find their way into the list by Kornman et al. (2014). That is, in particular, seminal papers by W.E.C. Moore and his coworkers [5].

Theme 2. Pathogenesis of periodontitis is modulated by various factors, including local, host, and environmental factors

There are only a handful of highly cited papers in the list but numerous “consensus papers of importance”. Only two out of eight highly cited papers explicitly dealt with the smoking epidemic, and eight out of  22 consensus papers of importance. The paper by Tomar and Asma (2000) [6], which suggested that more than 40% of periodontitis in the U.S. (based on finding of NHANES III) may be attributed to smoking, was at least quoted 548 times. That smoking can be regarded as a major causal contributing factor for the development of periodontitis has been suggested by numerous other authors on different continents. It is amazing that the paper by Hujoel et al. (2003) [7] who critically discuss the “hidden smoking epidemic” in the 20th century, has been quoted after all 63 times according to Google Scholar. Longitudinal studies on smokers and nonsmokers and, in particular, large intervention studies on the effect of smoking cessation on the development of periodontitis are more or less missing. In view of planned and already conducted  intervention studies on the effects of periodontal treatment on a number of systemic diseases and conditions where effects must be expected small and probably irrelevant, intervention studies on the effects of smoking cessation on periodontal health are overdue.

They may be much more pronounced than what can be achieved by non-surgical periodontal therapy targeting the dental biofilm. Of course, one has to take on the tobacco industry, something which is worth it anyway.

If time allows I will comment on the remaining themes in the coming days. So, stay tuned.


[1] Kornman KS, Robertson PB, Williams RC. The literature that shaped modern periodontology. J Periodontol 2014; 85: 3-9.

[2] Socransky SS. Criteria for the infectious agents in dental caries and periodontal disease. J Clin Periodontol 1979; 6: 16-21.

[3] Bradford Hill A. The environment and disease: association or causation? Proc Roy Soc Med 1965; 58: 295-300. [pdf]

[4] Hujoel P, Zina L, Cunha-Cruz J, Lopez R. Specific infections as the etiology of destructive periodontal disease: a systematic review. Eur J Oral Sci 2013; 121: 2-6.

[5] For instance, Moore WEC, Holdeman LV, Cato EP, Smibert RM, Burmeister JA, Palcanis KG, Ranney RR. Comparative bacteriology of juvenile periodontitis. Infect Immun  1985; 48: 507-519 (quoted 356 times); Moore WEC, Moore LH, Ranney RR, Smibert RM, Burmeister JA, Schenkein HA. The microflora of periodontal sites showing active destructive progression. J Clin Periodontol 1991; 18: 729-739 (quoted 232 times). Moore WEC. Microbiology of periodontal diseases. J Periodont Res 1987; 22: 335-341 (quoted 362 times). Data of these and other studies by the group were summarized in Moore WEC, Moore LVH. The bacteria of periodontal diseases. Periodontol 2000 1994; 5: 66-77 (quoted 760 times).

[6] Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol 2000; 71: 743-751.

[7] Hujoel PP, del Aquila MA, DeRouen TA, Bergström J. A hidden periodontitis epidemic during the 20th century? Community Dent Oral Epidemiol 2003; 31: 1-6.

22 January 2014 @ 4:39 pm.

Last modified August 21, 2014.



  1. Lynne Slim

    Hujoel is probably the sharpest tool in the periodontal shed~ he’s a professor, periodontist, biostatistician and epidemiologist. He, unlike others (and I won’t name names of individual/institutions) doesn’t exaggerate the perio/systemic links. Maybe that’s why he’s not cited as often as others.


Leave a Reply

Fill in your details below or click an icon to log in: Logo

You are commenting using your account. Log Out /  Change )

Google+ photo

You are commenting using your Google+ account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )


Connecting to %s