Progression of attachment loss is strongly associated with presence of the JP2 genotype of Aggregatibacter actinomycetemcomitans: A prospective cohort study of a young adolescent population

Journal of Clinical Periodontology

Volumn 41, Issue 3, 2014, Pages 232-241

  Höglund Åberg, Carola ^a   Kwamin, Francis ^b   Claesson, Rolf ^a   Dahlén, Gunnar ^c   Johansson, Anders ^a   Haubek, Dorte ^d  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF GHANA   (Ghana)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

A. actinomycetemcomitans; adolescent; attachment loss; Ghana; JP2 genotype; leukotoxin; periodontitis; progression

Indexed keywords

BACTERIAL TOXIN; CYTOTOXIN; EXOTOXIN; LEUKOTOXIN; VIRULENCE FACTOR;

ADOLESCENT; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; CLASSIFICATION; COHORT ANALYSIS; COMPARATIVE STUDY; DISEASE COURSE; FEMALE; FOLLOW UP; GENETICS; GENOTYPE; GHANA; HUMAN; MALE; MICROBIOLOGY; PATHOPHYSIOLOGY; PERIODONTAL DISEASE; PROSPECTIVE STUDY; RISK FACTOR; TOOTH PLAQUE;

ADOLESCENT; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; BACTERIAL TOXINS; COHORT STUDIES; CYTOTOXINS; DENTAL PLAQUE; DISEASE PROGRESSION; EXOTOXINS; FEMALE; FOLLOW-UP STUDIES; GENOTYPE; GHANA; HUMANS; MALE; PERIODONTAL ATTACHMENT LOSS; PROSPECTIVE STUDIES; RISK FACTORS; VIRULENCE FACTORS;

EID: 84893760560     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/jcpe.12209     Document Type: Article

References (44)

1. Åberg, C. H., Kwamin, F., Claesson, R., Johansson, A., &, Haubek, D., (2012) Presence of JP2 and non-JP2 genotypes of Aggregatibacter actinomycetemcomitans and attachment loss in adolescents in Ghana. Journal of Periodontology 83, 1520-1528.
2. Albandar, J. M., (2002) Global risk factors and risk indicators for periodontal diseases. Periodontology 2000 29, 177-206.
3. Brogan, J. M., Lally, E. T., Poulsen, K., Kilian, M., &, Demuth, D. R., (1994) Regulation of Actinobacillus actinomycetemcomitans leukotoxin expression: analysis of the promoter regions of leukotoxic and minimally leukotoxic strains. Infection and Immunity 62, 501-508.
4. Brown, L. J., Albandar, J. M., Brunelle, J. A., &, Löe, H., (1996) Early-onset periodontitis: progression of attachment loss during 6 years. Journal of Periodontology 67, 968-975.
5. Bueno, L. C., Mayer, M. P., &, DiRienzo, J. M., (1998) Relationship between conversion of localized juvenile periodontitis-susceptible children from health to disease and Actinobacillus actinomycetemcomitans leukotoxin promoter structure. Journal of Periodontology 69, 998-1007.
6. Cortelli, J. R., Cortelli, S. C., Jordan, S., Haraszthy, V. I., &, Zambon, J. J., (2005) Prevalence of periodontal pathogens in Brazilians with aggressive or chronic periodontitis. Journal of Clinical Periodontology 32, 860-866.
7. Darveau, R. P., (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nature Reviews. Microbiology 8, 481-490.
8. Elamin, A., Albandar, J. M., Poulsen, K., Ali, R. V., &, Bakken, V., (2011) Prevalence of Aggregatibacter actinomycetemcomitans in Sudanese patients with aggressive periodontitis: a case-control study. Journal of Periodontal Research 46, 285-291.
9. Fine, D. H., Kaplan, J. B., Kachlany, S. C., &, Schreiner, H. C., (2006) How we got attached to Actinobacillus actinomycetemcomitans: a model for infectious diseases. Periodontology 2000 42, 114-157.
10. Fine, D. H., Markowitz, K., Fairlie, K., Tischio-Bereski, D., Ferrendiz, J., Furgang, D., Paster, B. J., &, Dewhirst, F. E., (2013) A consortium of Aggregatibacter actinomycetemcomitans, Streptococcus parasanguinis, and Filifactor alocis is present in sites prior to bone loss in a longitudinal study of localized aggressive periodontitis. Journal of Clinical Microbiology 51, 2850-2861.
11. Fine, D. H., Markowitz, K., Furgang, D., Fairlie, K., Ferrandiz, J., Nasri, C., McKiernan, M., &, Gunsolley, J., (2007) Aggregatibacter actinomycetemcomitans and its relationship to initiation of localized aggressive periodontitis: longitudinal cohort study of initially healthy adolescents. Journal of Clinical Microbiology 45, 3859-3869.
12. Fives-Taylor, P. M., Meyer, D. H., Mintz, K. P., &, Brissette, C., (1999) Virulence factors of Actinobacillus actinomycetemcomitans. Periodontology 2000 20, 136-167.
13. Haraszthy, V. I., Hariharan, G., Tinoco, E. M., Cortelli, J. R., Lally, E. T., Davis, E., &, Zambon, J. J., (2000) Evidence for the role of highly leukotoxic Actinobacillus actinomycetemcomitans in the pathogenesis of localized juvenile and other forms of early-onset periodontitis. Journal of Periodontology 71, 912-922.
14. Haubek, D., (2010) The highly leukotoxic JP2 clone of Aggregatibacter actinomycetemcomitans: evolutionary aspects, epidemiology and etiological role in aggressive periodontitis. APMIS Supplementum 130, 1-53.
15. Haubek, D., DiRienzo, J. M., Tinoco, E. M. B., Westergaard, J., Lopez, N. J., Chung, C.-P., Poulsen, K., &, Kilian, M., (1997) Racial tropism of a highly toxic clone of Actinobacillus actinomycetemcomitans associated with juvenile periodontitis. Journal of Clinical Microbiology 35, 3037-3042.
16. Haubek, D., Ennibi, O. K., Poulsen, K., Benzarti, N., &, Baelum, V., (2004) The highly leukotoxic JP2 clone of Actinobacillus actinomycetemcomitans and progression of periodontal attachment loss. Journal of Dental Research 83, 767-770.
17. Haubek, D., Ennibi, O. K., Poulsen, K., Poulsen, S., Benzarti, N., &, Kilian, M., (2001) Early-onset periodontitis in Morocco is associated with the highly leukotoxic clone of Actinobacillus actinomycetemcomitans. Journal of Dental Research 80, 1580-1583.
18. Haubek, D., Ennibi, O.-K., Abdellaoui, L., Benzarti, N., &, Poulsen, S., (2002) Attachment loss in Moroccan early onset periodontitis patients and infection with the JP2-type of Actinobacillus actinomycetemcomitans. Journal of Clinical Periodontology 29, 657-660.
19. Haubek, D., Ennibi, O.-K., Poulsen, K., Vaeth, M., Poulsen, S., &, Kilian, M., (2008) Risk of aggressive periodontitis in adolescent carriers of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans in Morocco: a prospective longitudinal cohort study. Lancet 371, 237-242.
20. Haubek, D., Havemose-Poulsen, A., &, Westergaard, J., (2006) Aggressive periodontitis in a 16-year-old Ghanaian adolescent, the original source of Actinobacillus actinomycetemcomitans strain HK 1651- a 10-year follow up. International Journal of Paediatric Dentistry 16, 370-375.
21. Haubek, D., Poulsen, K., &, Kilian, M., (2007) Microevolution and patterns of dissemination of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infection and Immunity 75, 3080-3088.
22. Haubek, D., Poulsen, K., Westergaard, J., Dahlén, G., &, Kilian, M., (1996) Highly toxic clone of Actinobacillus actinomycetemcomitans in geographically widespread cases of juvenile periodontitis in adolescents of African origin. Journal of Clinical Microbiology 34, 1576-1578.
23. Haubek, D., &, Westergaard, J., (2004) Detection of a highly toxic clone of Actinobacillus actinomycetemcomitans (JP2) in a Moroccan immigrant family with multiple cases of localized aggressive periodontitis. International Journal of Pediatric Dentistry 14, 41-48.
24. Hayashida, H., Poulsen, K., &, Kilian, M., (2002) Differences in iron acquisition from human haemoglobin among strains of Actinobacillus actinomycetemcomitans. Microbiology 148, 3993-4001.
25. Henderson, B., Ward, J. M., &, Ready, D., (2010) Aggregatibacter (Actinobacillus) actinomycetemcomitans: a triple A* periopathogen? Periodontology 2000 54, 78-105.
26. Huang, Y., Kittichotirat, W., Mayer, M. P., Hall, R., Bumgarner, R., &, Chen, C., (2013) Comparative genomic hybridization and transcriptome analysis with a pan-genome microarray reveal distinctions between JP2 and non-JP2 genotypes of Aggregatibacter actinomyctemcomitans. Molecular Oral Microbiology 28, 1-17.
27. Hujoel, P., Zina, L., Cunha-Cruz, J., &, Lõpez, R., (2013) Specific infections as the etiology of destructive periodontal disease: a systematic review. European Journal of Oral Sciences 121, 2-6.
28. Johansson, A., (2011) Aggregatibacter actinomycetemcomitans leukotoxin: a powerful tool with capacity to cause imbalance in the host inflammatory response. Toxins 3, 242-259.
29. Kelk, P., Abd, H., Claesson, R., Sandström, G., Sjöstedt, A., &, Johansson, A., (2011) Cellular and molecular response of human macrophages exposed to Aggregatibacter actinomycetemcomitans leukotoxin. Cell Death & Disease 2, e126.
30. Kilian, M., Frandsen, E., Haubek, D., &, Poulsen, K., (2006) The etiology of periodontal disease revisited by population genetic analysis. Periodontology 2000 42, 158-179.
31. Kittichotirat, W., Bumgarner, R. E., Asikainen, S., &, Chen, C., (2011) Identification of the pangenome and its components in 14 distinct Aggregatibacter actinomycetemcomitans strains by comparative genomic analysis. PLoS One 6, e22420.
32. Lally, E. T., Hill, R. B., Kieba, I. R., &, Korostoff, J., (1999) The interaction between RTX toxins and target cells. Trends in Microbiology 7, 356-361.
33. Longo, P. L., Nunes, A. C., Umeda, J. E., &, Mayer, M. P., (2013) Gene expression and phenotypic traits of Aggregatibacter actinomycetemcomitans in response to environmental changes. Journal of Periodontal Research 48, 766-772.
34. Lõpez, R., Fernández, O., &, Baelum, V., (2006) Social gradients in periodontal diseases among adolescents. Community of Dental Oral Epidemiology 34, 184-196.
35. Macheleidt, A., Müller, H. P., Eger, T., Putzker, M., Fuhrmann, A., &, Zöller, L., (1999) Absence of an especially toxic clone among isolates of Actinobacillus actinomycetemcomitans recovered from army recruits. Clinical Oral Investigation 3, 161-167.
36. Mullally, B. H., (2004) The influence of tobacco smoking on the onset of periodontitis in young persons. Tobacco Induced Diseases 15, 53-65.
37. Munksgaard, P. S., Vorup-Jensen, T., Reinholdt, J., Söderström, C. M., Poulsen, K., Leipziger, J., Praetorius, H. A., &, Skals, M., (2012) Leukotoxin from Aggregatibacter actinomycetemcomitans causes shrinkage and P2X receptor-dependent lysis of human erythrocytes. Cellular Microbiology 14, 1904-1920.
38. Poulsen, K., Ennibi, O. K., &, Haubek, D., (2003) Improved PCR for detection of the highly leukotoxic JP2 clone of Actinobacillus actinomycetemcomitans in subgingival plaque samples. Journal of Clinical Microbiology 41, 4829-4832.
39. Socransky, S. S., &, Haffajee, A. D., (2005) Periodontal microbial ecology. Periodontology 2000 38, 135-187.
40. Timmerman, M. F., Van der Weijden, G. A., Abbas, F., Arief, E. M., Armand, S., Winkel, E. G., Van Winkelhoff, A. J., &, Van der Velden, U., (2000) Untreated periodontal disease in Indonesian adolescents. Longitudinal clinical data and prospective clinical and microbiological risk assessment. Journal of Clinical Periodontology 27, 932-942.
41. Tonetti, M. S., &, Claffey, N., (2005) Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. Group C Consensus report of the 5th European Workshop in periodontology. Journal of Clinical Periodontology 32, 210-213.
42. Van der Velden, U., Abbas, F., Armand, S., Loos, B. G., Timmerman, M. F., Van der Weijden, G. A., Van Winkelhoff, A. J., &, Winkel, E. G., (2006) Java project on periodontal diseases. The natural development of periodontitis: risk factors, risk predictors and risk determinants. Journal of Clinical Periodontology 33, 540-548.
43. Van der Velden, U., Abbas, F., Van Steenbergen, T. J., De Zoete, O. J., Hesse, M., De Ruyter, C., De Laat, V. H., &, De Graaff, J., (1989) Prevalence of periodontal breakdown in adolescents and presence of Actinobacillus actinomycetemcomitans in subjects with attachment loss. Journal of Periodontology 60, 604-610.
44. Wahasugui, T. C., Nakano, V., Piazza, R. M., &, Avila-Campos, M. J., (2013) Phenotypic and genotypic features of Aggregatibacter actinomycetemcomitans isolated from patients with periodontal disease. Diagnostic Microbiology and Infectious Disease 75, 366-372.