New views on periodontal microbiota in special patient categories

The microorganisms in periodontitis of special patient categories have been only partially elucidated. The periodontitis microbiota of HIV-infected individuals, cancer patients on myelosuppressive therapy, and persons with other medical disorders includes common suspected periodontal pathogens as well as enteric rods, pseudomonads, staphylococci and yeasts. Failing implants also may be associated with classical periodontal pathogens as well as primarily nonoral potential pathogens. Refractory periodontitis in systemically healthy adults can show a great variety of oral and nonoral organisms. The frequent occurrence of unusual periodontal organisms in special patient categories may be due to a weakened host response and/or usage of various chemotherapeutic regimens. The unusual organisms may contribute to progressive periodontitis and in leukemia patients may even give rise to life-threatening systemic manifestations. The primary therapeutic goal in special periodontitis patients is control of pathogens and amid the wide range of pathogenic microfloras, an effective treatment strategy should include a comprehensive microbiological analysis, especially if systemic antimicrobial therapy is contemplated.     

Periodontal diseases: current and future indications for local antimicrobial therapy

The microbial etiology of gingivitis and periodontitis provides the rationale for use of adjunctive antimicrobial agents in the prevention and treatment of periodontal diseases. Although mechanical removal of supra- and subgingival calcified and non-calcified plaque deposits has been proved effective to control the gingival inflammatory lesions as well as to halt the progression of periodontal attachment loss, some patients may experience additional benefits from the use of systemic or topical antimicrobial agents. Such agents are able to significantly affect supra- and subgingival plaque accumulation and/or suppress or eradicate periodontal pathogenic microflora. Currently, properly selected local antiseptic and systemic antibiotic therapies can provide periodontal treatment that is generally effective, low-risk and affordable. This paper will briefly review the host-related conditions in which the periodontal preventive and therapeutic approaches may be effectively assisted by a local antimicrobial regimen. Potential future indications for adjunctive local antimicrobial therapy will also be discussed.     

Prevalence and antimicrobial susceptibility of Enterobacteriaceae, Pseudomonadaceae and Acinetobacter in human periodontitis

This study examined the occurrence of non-oral gram-negative facultatively anaerobic rods in advanced adult periodontitis. Speciation and in vitro antimicrobial susceptibility testing was performed using the MicroScan micromethod system. A total of 42 taxa of Enterobacteriaceae, Pseudomonadaceae and Acinetobacter were isolated from 427 of 3,050 (14.0%) patients. In 159 (5.2%) patients, these organisms comprised more than 5% of the cultivable subgingival microflora. Enterobacter cloacae, Klebsiella pneumoniae, Pseudomonas aeruginosa, Klebsiella oxytoca and Enterobacter agglomerans accounted for more than 50% of all strains isolated. Virtually all study strains demonstrated high in vitro susceptibility to ciprofloxacin, but exhibited variable susceptibility patterns to 18 other antimicrobial agents tested. In 3 "refractory" periodontitis patients heavily infected with enteric rods, systemic ciprofloxacin therapy (500 mg BiD for 10 days) led to resolution of the subgingival infections and improved clinical periodontal status. The present findings indicate that 5% of severe periodontitis lesions may harbor high levels of non-oral, gram-negative, facultatively anaerobic rods. Systemic ciprofloxacin appears to be capable of eradicating these potential pathogens from deep periodontal pockets.     

Selection of antimicrobial agents in periodontal therapy

BACKGROUND: The recognition over the past 3 decades of microbial specificity in periodontitis has afforded dental practitioners the ability to prevent and treat the disease with a variety of antimicrobial drugs. These include systemic antibiotics, topical antibiotics and topical antiseptics. RESULTS: Systemic antibiotic therapy can be essential in eliminating pathogenic bacteria that invade gingival tissue and in helping control periodontal pathogens residing in various domains of the mouth from where they may translocate to periodontal sites. Frequently used periodontal combination antibiotic therapies are metronidazole-amoxicillin (250-375 mg of each 3 x daily for 8 days) and metronidazole-ciprofloxacin (500 mg of each 2 x daily for 8 days). Microbiological analysis helps determine the optimal antibiotic therapy and effectiveness of treatment. Topical antibiotics that are commercially available as controlled release devices suffer from several potential problems, including insufficient spectrum of antimicrobial activity in some periodontal polymicrobial infections, risks of producing an antibiotic resistant microbiota, and high acquisition costs. Topical antiseptics of relevance in periodontal treatment include 10% povidone-iodine placed subgingivally by a syringe for 5 min, and 0.1% sodium hypochlorite solution applied subgingivally by patients using an irrigation device. CLINICAL IMPLICATIONS: The present paper recommends periodontal treatment that includes a battery of professionally and patient-administered antimicrobial agents (properly prescribed systemic antibiotics, povidone-iodine and sodium hypochlorite subgingival irrigants, and chlorhexidine mouthrinse). Available chemotherapeutics can provide effective, safe, practical and affordable means of controlling subgingival colonization of periodontal pathogens and various types of periodontal disease.     

Change of antibiotic susceptibility following periodontal therapy. A pilot study in aggressive periodontal disease

BACKGROUND: The hypothesis was tested that bacterial susceptibilities in aggressive periodontitis change upon administration of systemic antibiotics as adjuncts to periodontal therapy. METHODS: In 23 subjects (average age 38.9+/-6.7 years) with aggressive periodontitis, microbial parameters were assessed prior to and 1 year after completion of comprehensive mechanical/surgical and systemic antimicrobial therapy. Following identification of five selected pathogens with the Rapid ID 32 A system, their susceptibilities towards amoxicillin/clavulanate potassium, metronidazole, and tetracycline were examined with the E-test. Antibiotics were administered according to the test results, and the minimal inhibitory concentrations (MIC90) were reevaluated after 1 year. Statistical analysis was performed on a patient basis, with the site data used for evaluation of the MIC levels. RESULTS: Bacterial MIC levels remained constant among the three antibiotic treatment groups compared with baseline. Mean MIC90 values ranged from <0.02 to 0.11 microg/ml (amoxicillin/clavulanate potassium), <0.02 to 0.27 microg/ml (metronidazole), and <0.02 to 0.11 microg/ml (tetracycline). Observed changes in susceptibility were attributed to the elimination of single bacterial taxa in the subgingival environment after antibiotic therapy. There were no statistically significant differences in clinical parameters among the treatment groups. Single tetracycline MICs were 1.5- to 6-fold enhanced compared to amoxicillin/clavulanate potassium and metronidazole. CONCLUSION: The periodontal pathogens investigated prior to and 1 year after periodontal therapy are tested sensitive to the antimicrobial agents. In aggressive periodontitis, changes in bacterial susceptibility upon the administration of systemic antibiotics are associated with the limited number of isolates tested following therapy.     

Antimicrobial profiles of periodontal pathogens isolated from periodontitis patients in The Netherlands and Spain

BACKGROUND AND AIM: Antimicrobial resistance of periodontal pathogens towards currently used antibiotics in periodontics has been investigated in a previous study. Microbial resistance in the periodontal microflora was more frequently observed in Spanish patients in comparison with Dutch patients. The aim of the present study was to compare antimicrobial susceptibility profiles of five periodontal bacteria isolated from periodontitis patients in Spain and in The Netherlands. MATERIAL AND METHODS: Subgingival plaque samples from adult patients with periodontitis were collected and cultured on selective and non-selective plates. Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, Fusobacterium nucleatum and Micromonas micros were isolated and used for minimal inhibitory concentration tests using the Epsilometer (E-test) technique. Eight different antibiotics were tested on all bacterial isolates. MIC50 and MIC90 values for each antibiotic and each species were determined and the percentage of resistant strains was calculated. RESULTS: Significantly higher MIC values were noted in Spanish strains of F. nucleatum for penicillin, ciprofloxacin, of P. intermedia for penicillin, amoxicillin and tetracycline, of M. micros for tetracycline, amoxicillin and azithromycin, and of P. gingivalis for tetracycline and ciprofloxacin. Based on breakpoint concentrations, a higher number of resistant strains in Spain were found in F. nucleatum for penicillin, amoxicillin and metronidazole, in Prevotella intermedia for tetracycline and amoxicillin, and in A. actinomycetemcomitans for amoxicillin and azithromycin. Resistance of P. gingivalis strains was not observed for any of the antibiotics tested both in Spain and The Netherlands. CONCLUSIONS: Differences exist in the susceptibility profiles of periodontal pathogens isolated from periodontitis patients in Spain and in The Netherlands. This implicates that antibiotic susceptibility testing is necessary to determine efficacy of antimicrobial agents. Also, clinical studies with antibiotics should take these differences into account. The information from the present study indicates that it may not be possible to develop uniform protocols for usage of antibiotics in the treatment of severe periodontitis in the European Union.     

Periodontal antimicrobials--finding the right solutions

Strengthened by promising research data and commercial backing, interest in the field of anti-infective periodontal therapy is rapidly expanding. Management of the periodontal microbiota with antibiotic drugs and antiseptic agents in conjunction with mechanical debridement seems to be more effective than mechanical therapy alone, at least in the treatment of advanced periodontal disease. The choice of a periodontal chemotherapeutic regimen requires an understanding of the usual infecting flora, available antimicrobial agents, and pathogen susceptibility patterns. Systemic administration of combinations of metronidazole and either amoxicillin or ciprofloxacin has been widely used with great success; however the presence of subgingival yeasts and resistant bacteria can be a problem in some periodontitis patients. Valuable antiseptic agents for subgingival application include 10% povidone-iodine for professional use and 0.1-0.5% sodium hypochlorite for patient self-care. These antiseptics have significantly broader spectra of antimicrobial action, are less likely to induce development of resistant bacteria and adverse host reactions, and are considerably less expensive than commercially available antibiotics in controlled release devices. In practice, mechanical debridement combined with subgingival povidone-iodine application in the dental office and sodium hypochlorite irrigation for patient self-care are valuable antimicrobial remedies in the treatment of virtually all types of periodontal disease. Management of moderate to severe periodontitis may require additional systemic antibiotic and/or surgical treatment.     

In vitro antimicrobial sensitivity of enteric rods and pseudomonads from advanced adult periodontitis

The prevalence and in vitro antimicrobial sensitivity of isolates of enteric rods and pseudomonads was examined in 844 adult periodontitis patients. These organisms were recovered from 13.5% of the study subjects. Ciprofloxacin exhibited the highest inhibitory activity of the 14 oral antimicrobial agents tested. Beta-lactam antibiotics were largely ineffective, and tetracycline failed to inhibit most Pseudomonas species. In vitro sensitivity data suggest that a subgingival microbiota comprising mainly streptococci would result from therapy that combined ciprofloxacin and metronidazole. Since streptococci may inhibit the growth of several putative periodontal pathogens, populations of "beneficial" streptococci in the periodontal pocket might constitute a very attractive therapeutic outcome. Controlled clinical studies are needed to clarify the possible role of ciprofloxacin in the treatment of destructive periodontitis.     

Changes in the prevalence of subgingival enteric rods, staphylococci and yeasts after treatment with penicillin and erythromycin

The changes in the balance of microbial flora in the periodontium after antibiotic treatment were investigated in a blind study. The prevalence of gram-negative enteric rods, staphylococci and yeasts was followed before and during penicillin or erythromycin treatment of 72 periodontitis patients without periodontal cleaning. The prevalence of subgingival coagulase-positive staphylococci increased significantly following systemic penicillin therapy. After systemic erythromycin therapy, the prevalence of subgingival gram-negative enteric rods increased. Ten of 24 (42%) patients receiving systemic penicillin therapy developed clinical evidence of periodontal abscesses. In the absence of conventional mechanical cleaning, systemic administration of penicillin and erythromycin antibiotic to patients with preexisting periodontitis may lead to periodontal superinfection with opportunistic organisms.     

Topical antimicrobial therapy and diagnosis of subgingival bacteria in the management of inflammatory periodontal disease

Bacterial specificity in human periodontal diseases suggests the possibility of diagnosing and treating periodontitis as specific infections and using microbiological diagnostic means to evaluate the efficacy of periodontal therapy. In a series of clinical trials, the usefulness of topical antimicrobial agents in combination with surgical and non-surgical conventional periodontal therapy were tested. The healing result was estimated by monitoring probing attachment levels (PAL). The usefulness of clinical and microbiological parameters to evaluate post-treatment healing result was tested. 9 of the patients exhibiting sites with recurrent periodontal disease were then evaluated for clinical and microbiological parameters to define accurate means to differentiate between active and inactive periodontal disease. The results showed that the frequency of periodontal lesions with significant loss of PAL after treatment was less in patients treated with antimicrobial agent. Specific microbiological parameters showed stronger correlation than clinical parameters with gain and/or loss of PAL post-treatment. Thus Actinobacillus actinomycetemcomitans and Bacteroides gingivalis occurred in periodontal lesions with progressing disease after treatment, but were rarely detected in samples from pockets of the same depths which did not exhibit further loss of PAL over a study period of 1 year. This study points to the usefulness of topical antimicrobial agent as an adjunct to mechanical subgingival debridement in the treatment of periodontitis in adults. The results also indicate the utility of diagnostic microbiology in the assessment of periodontal disease activity post-treatment.     

Antimicrobial activity of silver nitrate against periodontal pathogens

Metal ions were evaluated as potential antimicrobial agents suitable for local delivery in the oral cavity for the treatment of periodontitis. Silver nitrate, copper chloride, and zinc chloride were tested for antimicrobial activity in in vitro killing assays conducted in phosphate buffered saline with a series of oral bacteria including gram-negative periodontal pathogens and gram-positive streptococci. Copper and zinc salts failed to exhibit strong and consistent activity against periodontal pathogens. In contrast, silver at a concentration of 0.5 microg/mL produced a 3 log10 reduction in colony forming units (CFU)/mL or greater against all periodontal pathogens tested including Porphyromonas gingivalis, Prevotella intermedia, Prevotella denticola, Bacteroides forsythus, Fusobacterium nucleatum vincentii, Campylobacter gracilis, Campylobacter rectus, Eikenella corrodens, and Actinobacillus actinomycetemcomitans. In comparison, substantially higher concentrations of silver nitrate failed to kill oral streptococci. A silver nitrate concentration of 25 microg/mL produced log10 reductions in CFU/mL of 3.5-5 in killing assays performed in human serum against P. gingivalis, demonstrating the ability of silver to retain activity in a biological medium similar to that encountered in vivo in the periodontal pocket. These results identify silver nitrate, an antimicrobial that may possess advantages over traditional antibiotics, as a potential agent for controlled release local delivery in the oral cavity for the treatment of periodontitis.     

Primer for antimicrobial periodontal therapy

Successful prevention and treatment of periodontitis is contingent upon effective control of the periodontopathic microbiota. Periodontal pathogens reside in subgingival sites but also colonize supragingival plaque, tongue dorsum and other oral sites. Controlling destructive periodontal disease warrants a comprehensive antimicrobial approach that targets periodontal pathogens in various ecological niches of the oral cavity. Also, to effectively combat periodontal pathogens, the various elements of antimicrobial periodontal therapy should be engaged within a short period of time. Scaling and root planing, with or without periodontal surgery, along with proper oral hygiene, constitute the primary approach to controlling periodontopathogens. Antimicrobial agents administered systemically or locally can help suppress periodontal pathogens in periodontal sites and in the entire mouth. Microbiological testing aids the clinician in selecting the most effective antimicrobial agent or combination of agents, and in monitoring the effectiveness of periodontal treatment. The present paper considers theoretical and practical aspects of effective antimicrobial treatment of destructive periodontal disease.     

牙周优势厌氧菌耐药性的研究进展

牙周厌氧菌是造成牙周炎的主要因素。随着临床治疗中抗生素的滥用,牙周厌氧菌的耐药情况亦愈发普遍。本文就牙周优势厌氧菌及其耐药现状、耐药机制和耐药基因等研究进展作一综述,以期为临床合理使用抗菌药物和新抗菌药物的研发提供依据。     

Practical antimicrobial periodontal therapy

Specific pathogenic bacteria play a central role in the etiology and pathogenesis of destructive periodontal disease. Under suitable conditions, periodontal pathogens colonize the subgingival environment and are incorporated into a tenacious biofilm. Successful prevention and treatment of periodontitis is contingent on effective control of the periodontopathic bacteria, which is accomplished with professional treatment of diseased periodontal sites and patient performed plaque control. Subgingival mechanical debridement, with or without surgery, constitutes the basic means of disrupting the subgingival biofilm and controlling pathogens. Appropriate antimicrobial agents that can be administered systemically or via local delivery may enhance eradication or suppression of subgingival pathogens. Microbiological testing may aid the clinician in the selection of the most effective antimicrobial agent or combination of agents. Understanding the benefits and limitations of antibiotics and antiseptics will optimize their usefulness in combating periodontal infections.     

Antibiotic Resistance in Human Chronic Periodontitis Microbiota

Background: Patients with chronic periodontitis (CP) may yield multiple species of putative periodontal bacterial pathogens that vary in their antibiotic drug susceptibility. This study determines the occurrence of in vitro antibiotic resistance among selected subgingival periodontal pathogens in patients with CP. Methods: Subgingival biofilm specimens from inflamed deep periodontal pockets were removed before treatment from 400 adults with CP in the United States. The samples were cultured, and selected periodontal pathogens were tested in vitro for susceptibility to amoxicillin at 8 mg/L, clindamycin at 4 mg/L, doxycycline at 4 mg/L, and metronidazole at 16 mg/L, with a post hoc combination of data for amoxicillin and metronidazole. Gram‐negative enteric rods/pseudomonads were subjected to ciprofloxacin disk‐diffusion testing. Results: Overall, 74.2% of the patients with CP revealed subgingival periodontal pathogens resistant to at least one of the test antibiotics. One or more test species, most often Prevotella intermedia/nigrescens, Streptococcus constellatus, or Aggregatibacter actinomycetemcomitans, were resistant in vitro to doxycycline, amoxicillin, metronidazole, or clindamycin, in 55%, 43.3%, 30.3%, and 26.5% of the patients with CP, respectively. Fifteen percent of patients harbored subgingival periodontal pathogens resistant to both amoxicillin and metronidazole, which were mostly either S. constellatus (45 individuals) or ciprofloxacin‐susceptible strains of Gram‐negative enteric rods/pseudomonads (nine individuals). Conclusions: Patients with CP in the United States frequently yielded subgingival periodontal pathogens resistant in vitro to therapeutic concentrations of antibiotics commonly used in clinical periodontal practice. The wide variability found in periodontal pathogen antibiotic‐resistance patterns should concern clinicians empirically selecting antibiotic treatment regimens for patients with CP.     

Topical and systemic antibiotics in the management of periodontal diseases

Both systemic and topical antibiotics are increasingly used in the management of periodontal infections. Whilst these drugs are used mostly on an empirical basis, some contend that rational use of antibiotics should be the norm due to their wide abuse and consequential global emergence of antibiotic resistance organisms. Here we review the rationale and principles of antimicrobial therapy, treatment goals, drug delivery routes and various antibiotics that are used in the management of periodontal diseases. The pros and cons of systemic and local antibiotic therapy are described together with practical guidelines for their delivery. The available data indicate, in general, that mechanical periodontal treatment alone is adequate to ameliorate or resolve the clinical condition in most cases, but adjunctive antimicrobial agents, delivered either locally or systemically, can enhance the effect of therapy in specific situations. This is particularly true for aggressive (early onset) periodontitis, in patients with generalised systemic disease that may affect host resistance and in case of poor response to conventional mechanical therapy. Locally delivered antibiotics together with mechanical debridement are indicated for non-responding sites of focal infection or in localised recurrent disease. After resolution of the periodontal infection, the patient should be placed on an individually tailored maintenance care programme. Optimal plaque control by the patient is of paramount importance for a favourable clinical and microbiological response to any form of periodontal therapy.     

Use of antimicrobial agents during supportive periodontal therapy

Individual susceptibility to periodontal breakdown involves an interplay of genes, periodontal pathogens and other modulating factors. Anti-infective treatment, which includes oral hygiene measures, mechanical debridement, pharmacologic intervention and surgery, has been shown to be effective in arresting the progression of periodontal disease. Nevertheless, due to the chronic nature of the disease, susceptible individuals who are not maintained in a supervised recall program subsequent to the active treatment phase, show signs of recurrent destruction. Supportive periodontal therapy (SPT) is an integral part of periodontal treatment for patients with history of periodontitis, and is needed to prevent recurrence of disease in susceptible individuals. To prevent re-infection with periodontal pathogens, SPT includes elimination of dental plaque and bacteria from the oral cavity, thereby preventing the recurrence of pathogens into the gingival area. For individuals at risk of developing periodontitis, SPT should combine self-performed and professional anti-infective therapy, using mechanical and pharmacological means. The existing evidence suggests that the adjunctive use of antimicrobial pharmacologic therapy during SPT may enhance the results of mechanical debridement. The use of antimicrobials varies between patients, and is dependent on risk assessment and longitudinal monitoring of the clinical status of the periodontium.     

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??Objective    To discuss the influence of basic periodontal therapy on the levels of homocysteine??HCY??in serum and clinical periodontal parameters in patients with moderate to severe periodontitis at high risk of stroke. Methods      From January to October 2014??76 cases of patients with moderate to severe periodontitis at high risk of stroke who underwent treatment in Department of Stomatology or Neurology in People's Hospital of Liaoning Province were randomly divided into two groups. Forty cases in group A received basic periodontal treatment and neurology treatment??and 36 patients in group B only received neurology treatment. Another 36 patients with moderate to severe periodontitis were selected as group C??who received basic periodontal treatment. Observe the change of the HCY levels in serum and the clinical periodontal parameters??including bleeding on probing??BOP????probing depth??PD??and attachment loss??AL??. The data were analyzed by SPSS17.0 software package. Results    Compared with pre-treatment??the level of serum HCY and periodontal index of 3 groups decreased. Compared with B group??serum HCY in group A decreased in mean value??and periodontal index decreased more significantly. The difference was statistically significant??P < 0.05??. Conclusion    Basic periodontal treatment can reduce the level of serum HCY in patients with moderate to severe periodontitis at high risk of stroke and improve the body's inflammatory state??which may reduce the risk of high-risk stroke progressing to stroke.     

中重度牙周炎伴脑卒中高危人群牙周基础治疗效果观察

目的    探讨牙周基础治疗对中重度牙周炎伴脑卒中高危人群患者血清中同型半胱氨酸（HCY）炎症因子水平及临床牙周指标的影响。方法    选择2014年1—10月在辽宁省人民医院口腔科及神经内科就诊的中重度牙周炎伴脑卒中高危人群患者76例,随机分为2组：A组40例,接受牙周基础治疗+神经内科治疗;B组36例,仅接受神经内科治疗。另选取单纯中重度牙周炎患者36例,设为C组,接受牙周基础治疗。比较各组治疗前后血清HCY含量及探针出血（BOP）、牙周探诊深度（PD）、附着丧失（AL）等牙周指标的变化。采用SPSS17.0软件包对数据进行统计学分析。结果    与治疗前比较,3组患者血清HCY含量及各项牙周指标均下降。与B组相比,A组血清HCY含量均值较低,但两组差异无统计学意义（P > 0.05）;A组各项牙周指标下降更加明显,两组差异有统计学意义（P < 0.05）。结论    牙周基础治疗可降低中重度牙周炎伴脑卒中高危人群血清HCY水平,改善机体的炎症状态,可在一定程度上降低脑卒中高危人群向脑卒中发展的风险。     

Rapid antimicrobial resistance screening method for Bacteroides intermedius

The purpose of the study was to validate a rapid resistance screening (RRS) method for antimicrobial susceptibility testing of a selected periodontopathic microorganism using the standard broth dilution method as a control. Twenty-five subgingival plaque samples from gingivitis or periodontitis sites were plated on Trypticase soy agar supplemented with 5% rabbit blood with antibiotic discs (RRS method) and without (control). The antibiotics tested were: Augmentin, clindamycin, erythromycin, metronidazole, penicillin G and tetracycline hydrochloride. Bacteroides intermedius isolated from both groups of plates were placed onto antibiotic supplemented Trypticase soy broth. The antibiotic susceptibilities of B. intermedius isolated from the plates with antibiotic discs and the standard broth method were compared. The results showed high sensitivity and predictability for the RRS method compared with the control. The percentage of agreement was: 100% for Augmentin 30 micrograms, clindamycin 2 micrograms and tetracycline 30 micrograms; 96% for erythromycin 15 micrograms, metronidazole 80 micrograms and penicillin 10 IU; 92% for penicillin 2 IU; 88% for erythromycin 2 micrograms and 84% for tetracycline 5 micrograms. The results of this study document the feasibility of the RRS method for testing antimicrobial resistance of whole samples if its efficacy can be demonstrated for other bacteria. This method may be a quick and useful test for the periodontal practitioner in determining the antibiotic susceptibility of periodontal plaque pathogens.