Granulocyte-macrophage colony-stimulating factor (GM-CSF) in subjects with different stages of periodontitis according to the new classification

Dikilitas, Ahu; Karaaslan, Fatih; Aydin, Esra Özge; Yigit, Umut; Ertugrul, Abdullah Seckin

doi:10.1590/1678-7757-2021-0423

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Journal of Applied Oral Science

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Original Article • J. Appl. Oral Sci. 30 • 2022 • https://doi.org/10.1590/1678-7757-2021-0423 copy

Granulocyte-macrophage colony-stimulating factor (GM-CSF) in subjects with different stages of periodontitis according to the new classification

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Granulocyte-macrophage colony-stimulating factor (GM-CSF) is a multifunctional cytokine that regulates inflammatory responses in various autoimmune and inflammatory disorders. Objective: The purpose of this study was to analyze the gingival crevicular fluid (GCF) for GM-CSF, interleukin-1 beta (IL-1β), and macrophage inflammatory protein-1 alpha (MIP-1α) levels in patients with stage I, stage II, stage III, and stage IV periodontitis (SI-P, SII-P, SIII-P, and SIV-P). Methodology: A total of 126 individuals were recruited for this study, including 21 periodontal healthy (PH), 21 gingivitis (G), 21 SI-P, 21 SII-P, 21 SIII-P, and 21 SIV-P patients. Plaque index (PI), gingival index (GI), presence of bleeding on probing (BOP), probing depth (PD), and attachment loss (AL) were used during the clinical periodontal assessment. GCF samples were obtained and analyzed by an enzyme-linked immunosorbent assay (ELISA). Results: GCF GM-CSF, MIP-1α, and IL-1β were significantly higher in SII-P and SIII-P groups than in PH, G, and SI-P groups (p<0.05). There was no significant difference among the PH, G, and SI-P groups in IL-1β, GM-CSF, and MIP-1α levels (p>0.05). Conclusions: These results show that GM-CSF expression was increased in SII-P, SIII-P, and SIV-P. Furthermore, GM-CSF levels may have some potential to discriminate between early and advanced stages of periodontitis.

Keywords:
Periodontitis; Gingival crevicular fluid; Interleukins; Macrophages

Demographic variables	PH	G	SI-P	SII-P	SIII-P	SIV-P
	(n = 21)	(n = 21)	(n = 21)	(n = 21)	(n = 21)	(n = 21)
Age (years)	36 (30-48)	39 (30-40)	38 (30-41)	36 (30-44)	38 (28-42)	40 (36-48) ^* * p<0.05
Gender (female/male)	11 10	12 9	10 11	11 10	11 10	10 11
Number of teeth	27 (24-28)	26 (24-28)	26 (25-28)	26 (24-28)	25 (24-26)	25 (23-27)

		PH	G	SI-P	SII- P	SIII- P	SIV- P
		(n=21)	(n=21)	(n=21)	(n=21)	(n=21)	(n=21)
Full mouth	PD (mm)	1.8 (1.3-2.3)	2.2 (2-2.8)	4 (4-4.2)	4.1 (4-4.4)	6.5 (6.-6.8)	6.8 (6-7)
	AL (mm)	0 (0-0)	0 (0-0)	2 (1.5-2.5)	3 (2.5-4)	5 (5-5.8)	5.5 (5.2-6)
	GI	0.12 (0-0.4)	2 (1.6-2.2)	2 (1.6-2.2)	2.2 (1.2-3.1)	2.1 (1.2-3.1)	2.4 (2-2.8)
	BOP (%)	1.7 (1-2)	78.5 (58.2-88)	78 (71.6-80.2)	82.8 (78.6-88)	80 (71.6-88)	84.7 (80-86.7)
	PI	0.3 (0-0.7)	1.5 (1-2)	2.1 (1.6-2.9)	2.9 (2.1-3.3)	3 (2.2-3.2)	3 (2.9-3.2)
Sampling site	PD (mm)	2 (1.7-2.3)	3 (3-3)	4.4 (4-4.9)	5 (4.6-5.4)	6.7 (6-7.5)	7 (6-7.2)
	AL (mm)	0 (0-0)	0 (0-0)	2 (1.5-2.8)	3.5 (2.5-4)	5.5 (5-6)	5.8 (5.5-6)
	GI	0 (0-0)	2.2 (1.9-2.3)	2.3 (1.9-2.3)	2.3 (2.1-3.1)	2.3 (1.9-3.1)	2.5 (2.2-3.1)
	BOP (%)	0 (0-0)	100 (100-100)	100 (100-100)	100 (100-100)	100 (100-100)	100 (100-100)
	PI	0.2 (0.1-0.6)	2 (1-2.8)	2.6 (1.6-3.4)	3 (2.6-3.4)	3 (2.3-3.2)	3.2 (2.9-3.3)
Total amounts of biomarkers	GM-CSF (ng/30s)	0.59 (0.4-1)	0.62 (0.4-1.8)	0.58 (0.4-1.8)	1.15 (0.6-4.9)	1.55 (0.6-5.3)	1.02 (0.5-1.9)
	IL-1β (pg/30s)	4.07 (2.7-6.8)	3.94 (2.6-13.9)	5 (2.6-10.9)	14.31 (6.7-45.4)	15.09 (2.7-115)	36.78 (8.7-52.7)
	MIP-1α (pg/30s)	8.44 (6.3-11.8)	8.98 (6.3-18.3)	9.82 (7.2-12.6)	11.65 (6.5-27.9)	16.49 (6.5-21.3)	13.21 (8.3-28.2)

	Full mouth					Sampling site					Total amounts of bimarkers
	PI	GI	BOP	PD	AL	PI	GI	BOP	PD	AL	GM-CSF	IL-1β	MIP-1α
PH-G	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
PH-SI	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
PH-SII	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
PH-SIII	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
PH-SIV	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05
G-SI	0.001^* * p<0.05			0.001^* * p<0.05	0.001^* * p<0.05	0.003^* * p<0.05			0.001^* * p<0.05	0.001^* * p<0.05
G-SII	0.001^* * p<0.05		0.002^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
G-SIII	0.001^* * p<0.05		0.004^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05			0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
G-SIV	0.001^* * p<0.05	0.001^* * p<0.05	0.002^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05
SI-SII	0.001^* * p<0.05		0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05	0.005^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
SI-SIII	0.001^* * p<0.05		0.004^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.002^* * p<0.05			0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05
SI-SIV	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05	0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05		0.001^* * p<0.05	0.001^* * p<0.05
SII-SIII				0.001	0.001^* * p<0.05				0.001^* * p<0.05	0.001^* * p<0.05
SII-SIV	0,001^* * p<0.05	0,001^* * p<0.05		0,001^* * p<0.05	0,001^* * p<0.05		0,001^* * p<0.05		0,001^* * p<0.05	0,001^* * p<0.05
SIII-SIV		0,001^* * p<0.05			0,001^* * p<0.05		0,001^* * p<0.05			0,001^* * p<0.05

Clinical parameters		GM-CSF (ng/30s)	IL-1β (pg/30s)	MIP-1α (pg/30s)
Whole mouth
	PI	0.394**	0.450**	0.437**
	GI	0.244**	0.355**	0.287**
	BOP	0.278**	0.280**	0.326**
	PD	0.380**	0.553**	0.472**
	AL	0.411**	0.563**	0.519**
Sampling site
	PI	0.350**	0.414**	0.397**
	GI	0.251**	0.342**	0.351**
	BOP	0.245**	0.263**	0.293**
	PD	0.405**	0.561**	0.511**
	AL	0.422**	0.558**	0.504**

Biomarker	Clinical attachment loss^a a AL categories (mean full mounth AL): healthy/low: 0 to 2 mm; high/severe > 3.0 mm [37]				Statistics
levels	Unadjusted Scores		Adjusted Scores
	Healthy/Low	High/Severe	Healthy/Low	High/Severe	F^b b Adjusted for age, gender, and number of teeth; ANCOVA	p
	(n = 64)	(n = 62)	(n = 64)	(n = 62)
	mean±SD	mean±SD	mean±SD	mean±SD
GCSFR	0.66±0.28	1.63±1.16	0.53±0.12	0.76±0.12	48.635	0.001^* * p<0.05
IL-1B	5.07±2.56	25.53±21.77	5.95±2.1	24.65±2.1	33.746	0.001^* * p<0.05
MIP1-ALFA	9.11±2.04	14.59±6.14	9.17±0.6	14.53±0.6	33.712	0.001^* * p<0.05

	Univariable OR (95%Cl)^* * p<0.05	p-value
Age	1.17 (0.74-1.85)	0.497
Number of teeth	0.15 (0.04-0.6)	0.007^* * p<0.05
PI (sampling site)	29.54 (2.05- 425.16)	0.013^* * p<0.05
GM-CSF	56.83 (4.03-800.32)	0.003^* * p<0.05
MIP-1α	1.57 (1.09-2.27)	0.015^* * p<0.05

Faculdade De Odontologia De Bauru - USP Serviço de Biblioteca e Documentação FOB-USP, Al. Dr. Octávio Pinheiro Brisolla 9-75, 17012-901 Bauru SP Brasil, Tel.: +55 14 32358373 - Bauru - SP - Brazil
E-mail: jaos@usp.br

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[1] Corresponding address: Ahu Dikilitas, Usak University - Faculty of Dentistry - Department of Periodontology - Usak - Turkey. Phone: +90 05063569500 e-mail: ahu.dikilitas@usak.edu.tr