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Published in: BMC Oral Health 1/2009

Open Access 01-12-2009 | Research article

Periodontal conditions, oral Candida albicans and salivary proteins in type 2 diabetic subjects with emphasis on gender

Authors: Fawad Javed, Lena Klingspor, Ulf Sundin, Mohammad Altamash, Björn Klinge, Per-Erik Engström

Published in: BMC Oral Health | Issue 1/2009

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Abstract

Background

The association between periodontal conditions, oral yeast colonisation and salivary proteins in subjects with type 2 diabetes (T2D) is not yet documented. The present study aimed to assess the relationship between these variables in type 2 diabetic subjects with reference to gender.

Methods

Fifty-eight type 2 diabetic subjects (23 males and 35 females) with random blood glucose level ≥ 11.1 mmol/L were investigated. Periodontal conditions (plaque index [PI], bleeding on probing [BOP], probing pocket depth [PD] (4 to 6 mm and ≥ 6 mm), oral yeasts, salivary immunoglobulin (Ig) A, IgG and total protein concentrations, and number of present teeth were determined.

Results

Periodontal conditions (PI [p < 0.00001], BOP [p < 0.01] and PD of 4 to 6 mm [p < 0.001], salivary IgG (μg)/mg protein (p < 0.001) and salivary total protein concentrations (p < 0.05) were higher in type 2 diabetic females with Candida albicans (C. albicans) colonisation compared to males in the same group. Type 2 diabetic females with C. albicans colonisation had more teeth compared to males in the same group (p < 0.0001).

Conclusion

Clinical and salivary parameters of periodontal inflammation (BOP and IgG (μg)/mg protein) were higher in type 2 diabetic females with oral C. albicans colonisation compared to males in the same group. Further studies are warranted to evaluate the association of gender with these variables in subjects with T2D.
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Literature
1.
go back to reference Javed F, Näsström K, Benchimol D, Altamash M, Klinge B, Engström PE: Comparison of periodontal and socioeconomic status between subjects with type 2 diabetes mellitus and non-diabetic controls. J Periodontol. 2007, 78: 2112-2119. 10.1902/jop.2007.070186.CrossRefPubMed Javed F, Näsström K, Benchimol D, Altamash M, Klinge B, Engström PE: Comparison of periodontal and socioeconomic status between subjects with type 2 diabetes mellitus and non-diabetic controls. J Periodontol. 2007, 78: 2112-2119. 10.1902/jop.2007.070186.CrossRefPubMed
2.
go back to reference Rindum JL, Stenderup A, Holmstrup P: Identification of Candida albicans types related to healthy and pathological oral mucosa. J Oral Pathol Med. 1994, 23: 406-412. 10.1111/j.1600-0714.1994.tb00086.x.CrossRefPubMed Rindum JL, Stenderup A, Holmstrup P: Identification of Candida albicans types related to healthy and pathological oral mucosa. J Oral Pathol Med. 1994, 23: 406-412. 10.1111/j.1600-0714.1994.tb00086.x.CrossRefPubMed
3.
go back to reference Mese H, Matsuo R: Salivary secretion, taste and hyposalivation. J Oral Rehabil. 2007, 34: 711-723. 10.1111/j.1365-2842.2007.01794.x.CrossRefPubMed Mese H, Matsuo R: Salivary secretion, taste and hyposalivation. J Oral Rehabil. 2007, 34: 711-723. 10.1111/j.1365-2842.2007.01794.x.CrossRefPubMed
4.
go back to reference Urzua B, Hermosilla G, Gamonal J, Morales-Bozo I, Canals M, Barahona S, Coccola C, Cifuentes V: Yeast diversity in the oral microbiota of subjects with periodontitis: Candida albicans and Candida dubliniensis colonize the periodontal pockets. Med Mycol. 2008, 46 (8): 783-793. 10.1080/13693780802060899.CrossRefPubMed Urzua B, Hermosilla G, Gamonal J, Morales-Bozo I, Canals M, Barahona S, Coccola C, Cifuentes V: Yeast diversity in the oral microbiota of subjects with periodontitis: Candida albicans and Candida dubliniensis colonize the periodontal pockets. Med Mycol. 2008, 46 (8): 783-793. 10.1080/13693780802060899.CrossRefPubMed
5.
go back to reference Lyon JP, da Costa SC, Totti VMG, Munhoz MFV, dr Resende MA: Predisposing conditions for candida spp. Carriage in the oral cavity of denture wearers and individuals with natural teeth. Can J Microbiol. 2006, 52: 462-467. 10.1139/W05-148.CrossRefPubMed Lyon JP, da Costa SC, Totti VMG, Munhoz MFV, dr Resende MA: Predisposing conditions for candida spp. Carriage in the oral cavity of denture wearers and individuals with natural teeth. Can J Microbiol. 2006, 52: 462-467. 10.1139/W05-148.CrossRefPubMed
6.
go back to reference Dudko A, Kurnatowska AJ: Occurence of fungi in oral cavity of patients with periodontitis. Wiad Parazytol. 2007, 53: 295-300.PubMed Dudko A, Kurnatowska AJ: Occurence of fungi in oral cavity of patients with periodontitis. Wiad Parazytol. 2007, 53: 295-300.PubMed
7.
go back to reference Figueiral MH, Azul A, Pinto E, Fonseca PA, Branco FM, Scully C: Denture-related stomatitis: identification of aetiological and predisposing factors – a large cohort. J Oral Rehabil. 2007, 34: 448-455. 10.1111/j.1365-2842.2007.01709.x.CrossRefPubMed Figueiral MH, Azul A, Pinto E, Fonseca PA, Branco FM, Scully C: Denture-related stomatitis: identification of aetiological and predisposing factors – a large cohort. J Oral Rehabil. 2007, 34: 448-455. 10.1111/j.1365-2842.2007.01709.x.CrossRefPubMed
8.
go back to reference Hofman LF: Human saliva as a diagnostic specimen. J Nutr. 2001, 131 (Suppl 5): 1621S-1625S.PubMed Hofman LF: Human saliva as a diagnostic specimen. J Nutr. 2001, 131 (Suppl 5): 1621S-1625S.PubMed
9.
go back to reference Engström PE, George M, Larsson P, Lally ET, Taichman NS, Norhagen EG: Oral and systemic immunoglobulin G-subclass antibodies to Actinobacillus actinomycetemcomitans leukotoxin. Oral Microbiol Immunol. 1999, 14: 104-108. 10.1034/j.1399-302X.1999.140205.x.CrossRefPubMed Engström PE, George M, Larsson P, Lally ET, Taichman NS, Norhagen EG: Oral and systemic immunoglobulin G-subclass antibodies to Actinobacillus actinomycetemcomitans leukotoxin. Oral Microbiol Immunol. 1999, 14: 104-108. 10.1034/j.1399-302X.1999.140205.x.CrossRefPubMed
10.
go back to reference Javed F, Sundin U, Altamash M, Klinge B, Engström PE: Self-perceived oral health and salivary proteins in children with type 1 diabetes. J Oral Rehabil. 2009, 36: 39-44. 10.1111/j.1365-2842.2008.01895.x.CrossRefPubMed Javed F, Sundin U, Altamash M, Klinge B, Engström PE: Self-perceived oral health and salivary proteins in children with type 1 diabetes. J Oral Rehabil. 2009, 36: 39-44. 10.1111/j.1365-2842.2008.01895.x.CrossRefPubMed
11.
go back to reference Sandholm L, Tolo K, Olsen I: Salivary IgG, a parameter of periodontal disease activity? High responders to Actinobacillus actinomycetemcomitans Y4 in juvenile and adult periodontitis. J Clin Periodontol. 1987, 14: 289-294. 10.1111/j.1600-051X.1987.tb01535.x.CrossRefPubMed Sandholm L, Tolo K, Olsen I: Salivary IgG, a parameter of periodontal disease activity? High responders to Actinobacillus actinomycetemcomitans Y4 in juvenile and adult periodontitis. J Clin Periodontol. 1987, 14: 289-294. 10.1111/j.1600-051X.1987.tb01535.x.CrossRefPubMed
12.
go back to reference Anil S, Remani P, Beena VT, Nair RG, Vijayakumar T: Immunoglobulins in the saliva of diabetic patients with periodontitis. Ann Dent. 1995, 54: 30-33.PubMed Anil S, Remani P, Beena VT, Nair RG, Vijayakumar T: Immunoglobulins in the saliva of diabetic patients with periodontitis. Ann Dent. 1995, 54: 30-33.PubMed
13.
go back to reference Javed F, Altamash M, Klinge B, Engström PE: Periodontal conditions and oral symptoms in gutka-chewers with and without type 2 diabetes. Acta Odontol Scand. 2008, 66: 268-273. 10.1080/00016350802286725.CrossRefPubMed Javed F, Altamash M, Klinge B, Engström PE: Periodontal conditions and oral symptoms in gutka-chewers with and without type 2 diabetes. Acta Odontol Scand. 2008, 66: 268-273. 10.1080/00016350802286725.CrossRefPubMed
14.
go back to reference Addy M, Renton-Harper P: Local and systemic chemotherapy in the management of periodontal disease: an opinion and review of the concept. J Oral Rehabil. 1996, 23: 219-231. 10.1111/j.1365-2842.1996.tb00845.x.CrossRefPubMed Addy M, Renton-Harper P: Local and systemic chemotherapy in the management of periodontal disease: an opinion and review of the concept. J Oral Rehabil. 1996, 23: 219-231. 10.1111/j.1365-2842.1996.tb00845.x.CrossRefPubMed
15.
go back to reference Kadir T, Pisiriciler R, Akyüz S, Yarat A, Emekli N, Ipbüker A: Mycological and cytological examination of oral candidal carriage in diabetic patients and non-diabetic control subjects: thorough analysis of local aetiologic and systemic factors. J Oral Rehabil. 2002, 29: 452-457. 10.1046/j.1365-2842.2002.00837.x.CrossRefPubMed Kadir T, Pisiriciler R, Akyüz S, Yarat A, Emekli N, Ipbüker A: Mycological and cytological examination of oral candidal carriage in diabetic patients and non-diabetic control subjects: thorough analysis of local aetiologic and systemic factors. J Oral Rehabil. 2002, 29: 452-457. 10.1046/j.1365-2842.2002.00837.x.CrossRefPubMed
16.
go back to reference Scavini M, Stidley CA, Shah VO, Narva AS, Tentori F, Kessler DS, Bobelu A, Albert CP, Bobelu J, Jamon E, Natachu K, Neha D, Waikaniwa M, Welty TK, MacCluer JW, Zager PG: Prevalence of diabetes is higher among female than male Zuni Indians. Diabetes Care. 2003, 26: 55-60. 10.2337/diacare.26.1.55.CrossRefPubMed Scavini M, Stidley CA, Shah VO, Narva AS, Tentori F, Kessler DS, Bobelu A, Albert CP, Bobelu J, Jamon E, Natachu K, Neha D, Waikaniwa M, Welty TK, MacCluer JW, Zager PG: Prevalence of diabetes is higher among female than male Zuni Indians. Diabetes Care. 2003, 26: 55-60. 10.2337/diacare.26.1.55.CrossRefPubMed
17.
go back to reference Lambert TJ, Chapman LH: Consensus Working Group, Diabetic, psychotic disorders and antipsychotic therapy: a consequent statement. Med J Aust. 2004, 181: 544-548.PubMed Lambert TJ, Chapman LH: Consensus Working Group, Diabetic, psychotic disorders and antipsychotic therapy: a consequent statement. Med J Aust. 2004, 181: 544-548.PubMed
18.
go back to reference Nyomba BLG, Berard L, Murphy LJ: Facilitating access to glucometer reagents increases blood glucose self-monitoring frequency and improves glycaemic control: a prospective study in insulin-treated diabetic patients. Diabet Med. 2004, 21: 129-135. 10.1046/j.1464-5491.2003.01070.x.CrossRefPubMed Nyomba BLG, Berard L, Murphy LJ: Facilitating access to glucometer reagents increases blood glucose self-monitoring frequency and improves glycaemic control: a prospective study in insulin-treated diabetic patients. Diabet Med. 2004, 21: 129-135. 10.1046/j.1464-5491.2003.01070.x.CrossRefPubMed
19.
go back to reference Cohen M, Boyle E, Delaney C, Shaw J: A comparison of blood glucose meters in Australia. Diabetes Res Clin Pract. 2006, 71: 113-118. 10.1016/j.diabres.2005.05.013.CrossRefPubMed Cohen M, Boyle E, Delaney C, Shaw J: A comparison of blood glucose meters in Australia. Diabetes Res Clin Pract. 2006, 71: 113-118. 10.1016/j.diabres.2005.05.013.CrossRefPubMed
20.
go back to reference Knepp JH, Geahr MA, Forman MS, Valsamakis A: Comparison of automated and manual nucleic acid extraction methods for detection of enterovirus RNA. J Clin Microbiol. 2003, 4: 3532-3536. 10.1128/JCM.41.8.3532-3536.2003.CrossRef Knepp JH, Geahr MA, Forman MS, Valsamakis A: Comparison of automated and manual nucleic acid extraction methods for detection of enterovirus RNA. J Clin Microbiol. 2003, 4: 3532-3536. 10.1128/JCM.41.8.3532-3536.2003.CrossRef
21.
go back to reference Jalal S, Ciofu O, Høiby N, Gotoh N, Wretlind B: Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob Agents Chemother. 2000, 44: 710-712. 10.1128/AAC.44.3.710-712.2000.CrossRefPubMedPubMedCentral Jalal S, Ciofu O, Høiby N, Gotoh N, Wretlind B: Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob Agents Chemother. 2000, 44: 710-712. 10.1128/AAC.44.3.710-712.2000.CrossRefPubMedPubMedCentral
22.
go back to reference Gharizadeh B, Norberg E, Löffler J, Jalal S, Tollemar J, Einsele H, Klingspor L, Nyrén P: Identification of medically important fungi by the Pyrosequencing technology. Mycoses. 2004, 47: 29-33. 10.1046/j.1439-0507.2003.00949.x.CrossRefPubMed Gharizadeh B, Norberg E, Löffler J, Jalal S, Tollemar J, Einsele H, Klingspor L, Nyrén P: Identification of medically important fungi by the Pyrosequencing technology. Mycoses. 2004, 47: 29-33. 10.1046/j.1439-0507.2003.00949.x.CrossRefPubMed
23.
go back to reference Jonasson J, Olofsson M, Monstein HJ: Classification, identification and subtyping of bacteria based on pyrosequencing and signature matching of 16S rDNA fragments. APMIS. 2002, 110: 263-272. 10.1034/j.1600-0463.2002.100309.x.CrossRefPubMed Jonasson J, Olofsson M, Monstein HJ: Classification, identification and subtyping of bacteria based on pyrosequencing and signature matching of 16S rDNA fragments. APMIS. 2002, 110: 263-272. 10.1034/j.1600-0463.2002.100309.x.CrossRefPubMed
24.
go back to reference Navazesh M: Methods for collecting saliva. Ann N Y Acad Sci. 1993, 694: 72-77. 10.1111/j.1749-6632.1993.tb18343.x.CrossRefPubMed Navazesh M: Methods for collecting saliva. Ann N Y Acad Sci. 1993, 694: 72-77. 10.1111/j.1749-6632.1993.tb18343.x.CrossRefPubMed
25.
go back to reference Márton K, Boros I, Fejérdy P, Madléna M: Evaluation of unstimulated flow rates of whole and palatal saliva in healthy patients wearing complete dentures and in patients with Sjogren's syndrome. J Prosthet Dent. 2004, 91: 577-581. 10.1016/j.prosdent.2004.03.031.CrossRefPubMed Márton K, Boros I, Fejérdy P, Madléna M: Evaluation of unstimulated flow rates of whole and palatal saliva in healthy patients wearing complete dentures and in patients with Sjogren's syndrome. J Prosthet Dent. 2004, 91: 577-581. 10.1016/j.prosdent.2004.03.031.CrossRefPubMed
26.
go back to reference Ainamo J, Bay I: Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975, 25: 229-235.PubMed Ainamo J, Bay I: Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975, 25: 229-235.PubMed
27.
go back to reference Mühlemann HR, Son S: Gingival sulcus bleeding –a leading symptom in initial gingivitis. Helv Odontol Acta. 1971, 15: 107-113.PubMed Mühlemann HR, Son S: Gingival sulcus bleeding –a leading symptom in initial gingivitis. Helv Odontol Acta. 1971, 15: 107-113.PubMed
28.
go back to reference Taani DQ, Habashneh R, Hammad MM, Batieha A: The periodontal status of pregnant women and its relationship with socio-demographic and clinical variables. J Oral Rehabil. 2003, 30: 440-445. 10.1046/j.1365-2842.2003.01058.x.CrossRefPubMed Taani DQ, Habashneh R, Hammad MM, Batieha A: The periodontal status of pregnant women and its relationship with socio-demographic and clinical variables. J Oral Rehabil. 2003, 30: 440-445. 10.1046/j.1365-2842.2003.01058.x.CrossRefPubMed
29.
go back to reference Mata AD, Marques D, Rocha S, Francisco H, Santos C, Mesquita MF, Singh J: Effects of diabetes mellitus on salivary secretion and its composition in humans. Mol Cell Biochem. 2004, 261: 137-142. 10.1023/B:MCBI.0000028748.40917.6f.CrossRefPubMed Mata AD, Marques D, Rocha S, Francisco H, Santos C, Mesquita MF, Singh J: Effects of diabetes mellitus on salivary secretion and its composition in humans. Mol Cell Biochem. 2004, 261: 137-142. 10.1023/B:MCBI.0000028748.40917.6f.CrossRefPubMed
30.
go back to reference Bernardi MJ, Reis A, Loguercio AD, Kehrig R, Leite MF, Nicolau J: Study of the buffering capacity, pH and salivary flow rate in type 2 well-controlled and poorly controlled diabetic patients. Oral Health Prev Dent. 2007, 5: 73-78.PubMed Bernardi MJ, Reis A, Loguercio AD, Kehrig R, Leite MF, Nicolau J: Study of the buffering capacity, pH and salivary flow rate in type 2 well-controlled and poorly controlled diabetic patients. Oral Health Prev Dent. 2007, 5: 73-78.PubMed
31.
go back to reference Inoue H, Ono K, Masuda W, Morimoto Y, Tanaka T, Yokota M, Inenaga K: Gender difference in unstimulated whole saliva flow rate and salivary gland sizes. Arch Oral Biol. 2006, 51: 1055-1060. 10.1016/j.archoralbio.2006.06.010.CrossRefPubMed Inoue H, Ono K, Masuda W, Morimoto Y, Tanaka T, Yokota M, Inenaga K: Gender difference in unstimulated whole saliva flow rate and salivary gland sizes. Arch Oral Biol. 2006, 51: 1055-1060. 10.1016/j.archoralbio.2006.06.010.CrossRefPubMed
32.
go back to reference Hujoel PP, White BA, García RI, Listgarten MA: The dentogingival epithelial surface area revisited. J Periodontal Res. 2001, 36: 48-55. 10.1034/j.1600-0765.2001.00011.x.CrossRefPubMed Hujoel PP, White BA, García RI, Listgarten MA: The dentogingival epithelial surface area revisited. J Periodontal Res. 2001, 36: 48-55. 10.1034/j.1600-0765.2001.00011.x.CrossRefPubMed
33.
go back to reference Wang J, Ohshima T, Yasunari U, Namikoshi S, Yoshihara A, Miyazaki H, Maeda N: The carriage of Candida species on the dorsal surface of the tongue: the correlation with the dental, periodontal and prosthetic status in elderly subjects. Gerodontology. 2006, 23: 157-163. 10.1111/j.1741-2358.2006.00130.x.CrossRefPubMed Wang J, Ohshima T, Yasunari U, Namikoshi S, Yoshihara A, Miyazaki H, Maeda N: The carriage of Candida species on the dorsal surface of the tongue: the correlation with the dental, periodontal and prosthetic status in elderly subjects. Gerodontology. 2006, 23: 157-163. 10.1111/j.1741-2358.2006.00130.x.CrossRefPubMed
34.
go back to reference Yamanaka K, Nakagaki H, Morita I, Maeda N, Ohara H, Tomatsu S, Nakashima T, Watanabe Y, Ohta N, Shibata K: Relationship between oral Candida species and risk factors with reference to drugs with xerostomic side effects among institutionalised elderly in Aichi Pref., Japan. Community Dent Health. 2005, 22: 19-24.PubMed Yamanaka K, Nakagaki H, Morita I, Maeda N, Ohara H, Tomatsu S, Nakashima T, Watanabe Y, Ohta N, Shibata K: Relationship between oral Candida species and risk factors with reference to drugs with xerostomic side effects among institutionalised elderly in Aichi Pref., Japan. Community Dent Health. 2005, 22: 19-24.PubMed
35.
go back to reference Ship JA, Vissink A, Challacombe SJ: Use of prophylactic antifungals in the immunocompromised host. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007, 103 (Supp1 l): S6.e1-14. 10.1016/j.tripleo.2006.11.003. Ship JA, Vissink A, Challacombe SJ: Use of prophylactic antifungals in the immunocompromised host. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007, 103 (Supp1 l): S6.e1-14. 10.1016/j.tripleo.2006.11.003.
36.
go back to reference Lockhart SR, Joly S, Vargas K, Swails-Wenger J, Enger L, Soll DR: Natural defenses against Candida colonization breakdown in the oral cavities of the elderly. J Dent Res. 1999, 78: 857-868. 10.1177/00220345990780040601.CrossRefPubMed Lockhart SR, Joly S, Vargas K, Swails-Wenger J, Enger L, Soll DR: Natural defenses against Candida colonization breakdown in the oral cavities of the elderly. J Dent Res. 1999, 78: 857-868. 10.1177/00220345990780040601.CrossRefPubMed
37.
go back to reference Aizen E, Feldman PA, Madeb R, Steinberg J, Merlin S, Sabo E, Perlov V, Srugo I: Candida albicans colonization of dental plaque in elderly dysphagic patients. Isr Med Assoc J. 2004, 6: 342-345.PubMed Aizen E, Feldman PA, Madeb R, Steinberg J, Merlin S, Sabo E, Perlov V, Srugo I: Candida albicans colonization of dental plaque in elderly dysphagic patients. Isr Med Assoc J. 2004, 6: 342-345.PubMed
38.
go back to reference Ono K, Morimoto Y, Inoue H, Masuda W, Tanaka T, Inenaga K: Relationship of the unstimulated whole saliva flow rate and salivary gland size estimated by magnetic resonance image in healthy young humans. Arch Oral Biol. 2006, 51: 345-349. 10.1016/j.archoralbio.2005.09.001.CrossRefPubMed Ono K, Morimoto Y, Inoue H, Masuda W, Tanaka T, Inenaga K: Relationship of the unstimulated whole saliva flow rate and salivary gland size estimated by magnetic resonance image in healthy young humans. Arch Oral Biol. 2006, 51: 345-349. 10.1016/j.archoralbio.2005.09.001.CrossRefPubMed
Metadata
Title
Periodontal conditions, oral Candida albicans and salivary proteins in type 2 diabetic subjects with emphasis on gender
Authors
Fawad Javed
Lena Klingspor
Ulf Sundin
Mohammad Altamash
Björn Klinge
Per-Erik Engström
Publication date
01-12-2009
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2009
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/1472-6831-9-12

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