Influence of moderate to severe chronic periodontitis on dental pulp.

BACKGROUND: The relationship between periodontal disease and dental pulp changes is controversial and has been debated for many years. This human study was performed to evaluate the possible effects of moderate to advanced periodontal disease on the different aspect of dental pulp structure.
MATERIALS AND METHODS: Twenty hopeless permanent teeth were extracted from systemically healthy adults because of moderate to advanced chronic periodontitis, with a bone loss of >6 mm and a mobility of grade 2 or 3. Upon extraction, the apical 2 to 3 mm of the roots were immediately sectioned. Four to five sections were mounted on each slide, and every third slide was stained with hematoxylin and eosin. The specimens were histologically processed and examined by an oral pathologist.
RESULTS: Non-inflamed pulp, with partial or complete necrosis in some sections and several non-necrotic sections, was found in only 6.3% of teeth. Most teeth (58.3%) displayed edematous pulps. Slightly fibrotic pulps were seen in 52.1% of sections. Odontoblastic integrity was seen in 31.3% of teeth. Most teeth (77.1%) displayed no pulp stones. In 43.8% of teeth, the pulp vessels displayed dilatation.
CONCLUSIONS: Moderate to advanced periodontal disease can affect the dental pulp. Careful consideration of diagnostic and treatment planing in patients with endodontic-periodontal involvement is therefore recommended.

INTRODUCTION

Dental pulp communicates with the periodontium through apical, lateral, or accessory canals. Studies in human beings and in experimental animal models have shown that pulpal pathosis can cause varying degrees of periodontal changes.[1] Following successful root canal therapy, pathologic changes of endodontic origin usually disappear, and the periodontium returns to normal.[2] However, the interrelationship of periodontal disease and pulpal pathosis is controversial, with several opposing and apparently irreconcilable lines of evidence being supported in the literature.[3]

For example, the pulps of teeth with longstanding periodontal disease have been shown to exhibit fibrosis and intrapulpal mineralization.[4] Based on a superficial review of the literature and on four clinical cases, Serene (1967) concluded that periodontium destruction resulted in the contamination of many teeth.[5] However, other studies have shown no correlation between the periodontal disease severity and morphologic changes of the pulp tissue.[6]

The purpose of the present study was to address the controversy surrounding the relationship between periodontal disease and pulpal tissue changes. To examine the degree to which pulpal pathosis is associated with periodontal disease, we evaluated the pulp of teeth affected by moderate to severe chronic periodontitis. To eliminate causation by other complications such as decay, operative procedures, or periodontal manipulation, cases with a history of periodontal therapy were excluded and the histologic preparation was designed to differentiate fixation artifacts from true pathosis.

MATERIALS AND METHODS

Twenty human teeth with chronic periodontitis were extracted from patients with mean age of 44.1 (±5.8) years. Teeth were extracted at the Periodontics Department of the Mashhad School of Graduate Dentistry. The patients in this report signed consent forms to participate in this study. Chronic periodontitis was diagnosed based on the criteria of the American Academy of Periodontology (1999).[7] Pulp tissue samples were obtained from 20 single roots from the extracted teeth. Only intact teeth were used. The extracted teeth exhibited a bone loss of >6 mm, crown-to-root ratio of >1:1, no caries or fillings, and no history of operative manipulation, trauma, or bruxism. Each patient was systemically healthy and was not taking any medication.

Before extraction, each tooth was carefully periodontally and endodontically documented. No gingival recession was noted. If the tooth was diagnosed as hopeless, the treatment of choice was extraction with either a bridge or ridge augmentation and an implant. Periodontal assessment was performed by measuring the periodontal pocket depth, soft-tissue recession, and degree of mobility of each tooth. The extracted teeth displayed mobility grades of 2 or 3. All samples used in this study had natural periodontal involvement.

Using local anesthesia, the teeth were extracted as non-traumatically as possible to prevent the histological sequelae of traumatic extraction. The histological technique used was one commonly employed by the Mashhad School of Graduate Dentistry. Immediately following extraction, the apical 2 to 3 mm of the roots were sectioned with a No. 701 fissure bur. Access to the pulp tissue was gained with a high-speed hand piece under a constant flow of cool water. Teeth were placed into 10% neutral buffered formalin solution. After incubation for at least 7 days, the teeth were decalcified in 8% chloridric acid for 30 days. The specimens were histologically processed, embedded in paraffin, and serially sectioned using a microtome set at 5-pm thickness. The roots were arbitrarily divided into the coronal third, middle third, and apical third zones. Four to five sections were mounted on each slide, and every third slide was stained with hematoxylin and eosin (H and E). From the 20 sample teeth, four specimens were excluded during processing, leaving 16 teeth for histological evaluation. The sections were later examined by the authors and an oral pathologist. A single experienced oral pathologist reviewed the slides.

Microscopic examination of each section was made (Model SE, Nippon KOGAKU K.K, Japan). After observing all serial sections of each specimen, the relative degree of inflammation, amount of fibrosis, presence of pulp stones, presence of edema, condition of pulpal vessels, and odontoblastic integrity were recorded [Figure 1]. The relative degree of inflammation was graded as follows: no inflammation (0-2 infiltrating cells); light inflammation (2-5 infiltrating cells); moderate inflammation (5-10 infiltrating cells); or severe inflammation (>10 infiltrating cells). Fibrosis was defined as an increased fibroblast and collagen fiber concentration. The relative degree of fibrosis was graded as follows: light fibrosis (3-10 fibroblast cells); moderate fibrosis (11-30 fibroblast cells); or severe fibrosis (≥31 fibroblast cells). Necrotic specimens were categorized by whether the necrosis was partial or complete. The vessels were categorized into three groups (normal, atrophied, or dilated), according to their size. Edema was defined as the accumulation of interstitial fluids in pulp.

Figure 1

Representative section of pulp tissue from a tooth with chronic periodontitis (a) Note the moderate to severe inflammation, H and E staining, ×100 (b) Note the complete necrosis, H and E staining, ×40 (c) Note the edema, H and E staining, ×100 (d) Note the severe fibrosis, H and E staining, ×100 (e) Note the increased thickness of predentin, H and E staining, ×100 (f) Note the odontoblastic integrity, H and E staining, ×100 (g) Note the pulp stones, H and E staining, ×40 (h) Note the complete necrosis, H and E staining, ×40

RESULTS

The mean age of participants in the study was 42.8 years. Histological sections were evaluated by microscopy, regardless of clinical results. Several microscopic sections indicated that the pulp could range from intact to necrotic in different sections of the same tooth.

Inflammation was a common finding in the samples, with only 6.3% of teeth showing no inflammation. The inflammation was mild in most sections and always chronic. Pulps with necrosis (partial or complete) were seen in different sections. Several sections had no necrosis (35.4%). Partial necrosis (41.7%) was more common than complete necrosis (22.9%). Most teeth displayed edematous pulps (58.3%). Pulps with slight fibrosis were seen in many sections (52.1%), with only 6.3% of samples showing no fibrosis. A majority of teeth (68.8%) also displayed a loss of odontoblastic integrity. Pulp stones were absent in 77.1% of teeth. Finally, although the pulp vessels were dilated in most teeth (43.8%), atrophic changes or intact vessels were also seen [Table 1].

Table 1

Histologic evaluation of teeth with chronic periodontitis

DISCUSSION

In our study, we showed that moderate to severe chronic periodontitis can affect the dental pulp. Inflammation, fibrosis, edema, reduced predentine thickness, and missing odontoblastic integrity are the observed changes. Evidence for the effect of periodontal disease on the pulp has mainly been based on anatomic and circulatory interrelationships. Pulps subjected to a combination of irritants (e.g., caries, fillings, or both) and periodontal disease show an increased incidence of pulp degeneration, inflammation, and necrosis compared to teeth with periodontal disease alone. Periodontal disease produces inflammatory lesions in both the apical and radicular areas of the pulp. The latter are usually associated with a lateral canal communicating with the periodontal lesion. Therefore, secondary pulpitis can be caused by periodontal lesions.[1]

Pulp with partial or complete necrosis was seen in various sections, although several sections displayed no necrosis. Pressure from the mobility of the periodontally involved teeth may underlie the observed changes. The greatest reactions in the pulp to inflammatory or atrophic changes appear to be related to the presence of excessive numbers of accessory and lateral canals. Therefore, these canals seem to have an effect on the status of the pulp in periodontally involved teeth.[1] The interference of the blood supply through the lateral canals along the root sides may mediate the observed inflammation and pulp necrosis. Toxic products entering through the lateral canals can also produce inflammatory responses in the pulp.[1] Microorganisms present in the periodontal lesions may injure the pulp cells through their metabolic products. Moreover, the entry of microorganisms through the lateral canals may explain the persistence of positive cultures in endodontic procedures.[8]

Pulps with slight fibrosis were common. Fibrosis is frequently mentioned in connection with aging and chronic irritation of the pulp through long function. However, studies indicate that the amount of collagen does not increase perceptibly in the radicular pulp after the age of 39 years.[9] Furthermore, age is not consistently linked to pulpal calcification,[10] and pulpal changes found in older patients are not further advanced or more severe than those seen in young patients.[11] Thus, age per se cannot be regarded as the causative factor for the observed pulpal changes.[1213]

Most teeth displayed no pulp stones, similar to previous results.[14] Rubach WC and Mitchell DF observed that denticles were most common in the coronal pulp, and took a variety of forms, from diffuse to concentric laminated bodies. Serial sections revealed that many of the structures appearing as free pulp stones were actually projections of primary or, more often, secondary dentine from the internal pulpal wall, sectioned in such a plane as to make them appear as free denticles. The presence of surrounding odontoblasts indicated that such structures were dentine.[10]

Most of the teeth displayed dilated pulpal vessels, although in other teeth atrophic changes and intact vessels were also seen. The vessels varied considerably in diameter, and no clear distinction could be made between afferent and efferent vessels. Rubach WC and Mitchell DF observed that the vessels were filled with erythrocytes and white blood cells in an apparently normal ratio.[10] Despite the observed vessel dilatation, nonedematous pulp was seen in most teeth. Ekblom and Hansson (1984) showed that fenestrated capillaries were most frequently observed in the odontoblastic region.[15]

Most teeth displayed some amount of pulpal inflammation. Similarly, a previous study of periodontically involved teeth showed that all pulpal sections displayed a generalized infiltration of inflammatory cells, including frequent lymphocytes, plasma cells, and macrophages with a few polymorphonuclear leukocytes.[14] Artifacts due to an uncommon direction of the odontoblastic sectioning may account for some of the reported inflammation in sound teeth. When viewed in cross section, odontoblasts appear similar to lymphocytes. If a denticle or the surface of secondary dentine was positioned in such a way that the knife edge caught only the neighboring odontoblasts, then the teeth would appear inflamed.[10]

Many of the pulpal pathologies reported in previous studies also involved degenerative conditions (i.e., reticular atrophy, “fatty degeneration, etc.).[16] Thus, the observed alterations may not reflect true pathosis, but rather poor fixation of the dental pulp.[10] In addition, it is unclear in these past studies whether the periodontally diseased teeth had received previous treatment. Extensive periodontal manipulation may compromise the pulp health. In our investigation, pulpal changes cannot be attributed to local irritants, since the selected teeth were unfilled and free of caries. It is generally accepted that pulpal changes may occur if more than half the thickness of the enamel is abraded. Since the teeth used in this study showed minimal amounts of attrition, this factor cannot be regarded as the cause of the observed changes.[11]

A previous study using rat teeth demonstrated pulp damage due to gingiva stripping from the alveolar crest.[17] In 1963, Seltzer and others introduced the concept of “retrograde pulpitis.” Through interference with the nutritional supply, periodontal lesions routinely produced atrophic and degenerative changes in the pulps of involved teeth.[10] Another well-documented study of periodontal disease concluded that pulpitis and/or necrosis could result from periodontal inflammation.[10] However, no normal control teeth from the same mouth were used, and no mention was made of a previous history of periodontal therapy.

Seltzer and Bender (1972) found that human teeth subjected to a combination of pulpal and periodontal irritants had a greater incidence of inflammatory reactions than teeth with periodontal disease alone.[1] Grajewska (1997) found many pulp stones and also large denticles in several human cases of periodontal disease.[18] Nemec et al. (2007) also showed the advanced periodontitis affecting teeth and findings specific to periodontally affected teeth included acute and chronic pulpitis, vascular congestion, and pulp necrosis.[19]

In contrast with the several studies that confirmed our observations, many other studies have reported conflicting results.[61120] An extensive and well-controlled study by Maslur and Massler found no effect of the severity or presence of periodontal disease on the pulp, with similar mild to severe pulp histologic changes being observed in both healthy control and periodontally affected teeth.[11] Czarnecki and Schilder (1979) claimed that pulpal pathosis is often associated with deep decay or extensive restoration. They observed no correlation between periodontal disease severity and the presence of pulpal pathosis, with normal pulps being seen in teeth with advanced periodontal disease.[20] The clinical and histological examination of 25 teeth of a patient with varying degrees of attachment loss due to periodontal disease revealed no correlation between the severity of periodontal disease and morphologic changes of the pulp tissue.[6]

This brief literature review shows that the influence of periodontal disease on the dental pulp has been approached from various angles. It is unclear whether the changes observed were limited to diseased teeth, or whether they would also be observed in other teeth from the same patient. Indeed, it is difficult to prepare a control group in human studies of periodontal disease. Ideally, the control and test teeth should be extracted from one person. However, healthy teeth are generally extracted for orthodontic reasons, particularly in adolescence. It is rare that one person will simultaneously have both hopeless teeth from severe periodontitis and healthy teeth to be extracted. Therefore, controlled studies have largely been confined to animal models. Observed discrepancies between previous results and those presented here may be due to the use of different criteria for the histological and clinical evaluation of the pulp tissue, or to the lack of similar documentation of clinical periodontal disease parameters.

In conclusion, our results indicate that moderate to severe chronic periodontitis can affect the dental pulp. Careful consideration of diagnostic and treatment planning in patients with endodontic-periodontal involvement is therefore recommended.