伴与不伴糖尿病的牙周炎患者牙周基础治疗的疗效比较及其与白细胞水平的相关分析

doi:10.19723/j.issn.1671-167X.2022.01.008

摘要/Abstract

摘要：

目的: 比较伴与不伴糖尿病的牙周炎患者牙周基础治疗的临床疗效差异,并分析两组患者牙周基础治疗与白细胞水平的相关性。方法: 纳入无系统性疾病的慢性牙周炎患者32例(CP组),伴2型糖尿病的慢性牙周炎患者27例(CP+DM组)。所有患者行全口牙周检查和空腹血液检查,记录患者入院时的数据作为基线资料,包括探诊深度(probing depth, PD)、附着丧失(attachment loss, AL)、出血指数(bleeding index, BI)、菌斑指数(plaque index, PLI)、白细胞(white blood cell, WBC)计数和空腹血糖(fasting blood glucose, FBG),CP+DM组额外记录糖化血红蛋白(hemoglobin A1c, HbA1c)。对所有患者进行牙周基础治疗,治疗后3个月和6个月时重复入院时的所有检查。比较两组治疗前后牙周临床指标及血液指标的变化差异,采用广义线性混合模型分析WBC与牙周临床指标及糖代谢指标的相关性。结果: 入院时两组患者的牙周炎症和破坏程度一致,但CP+DM组WBC水平显著高于CP组[(7.14±1.99)×10⁹/L vs. (6.01±1.26)×10 ⁹/L, P=0.01]。牙周基础治疗3个月及6个月后,两组患者的全口平均PD、AL、BI及PLI均显著低于入院时基线水平,且6个月时CP+DM组的PD比3个月时仍有进一步降低[(3.33±0.62) mm vs. (3.61±0.60) mm,P<0.05]。治疗后3个月和6个月相比,两组各项牙周指标之间差异无统计学意义。CP+DM组治疗后3个月和6个月的HbA1c水平均显著低于基线水平[(7.09±0.79)% vs. (7.64±1.16)%,P<0.05;(7.06±0.78)% vs. (7.64±1.16)%,P<0.05], 6个月时的FBG显著低于基线水平[(7.35±1.14) mmol/L vs. (8.40±1.43) mmol/L,P<0.05]。CP组的WBC水平在治疗后3个月时显著低于基线水平[(5.35±1.37)×10 ⁹/L vs. (6.01±1.26)×10 ⁹/L,P<0.05],CP+DM组的WBC水平在治疗后6个月时显著低于基线水平[(6.00±1.37)×10⁹/L vs. (7.14±1.99)×10 ⁹/L,P<0.05]。广义线性混合模型分析显示,WBC水平与PD及FBG呈一定程度正相关。结论: 牙周基础治疗均能有效改善伴与不伴2型糖尿病的慢性牙周炎患者的牙周状况,有利于糖尿病患者的血糖控制,但糖尿病患者的牙周指标及WBC水平对牙周基础治疗的反应慢于不伴糖尿病的患者,WBC在糖尿病与牙周炎的相互关联中有重要意义。

关键词: 牙周炎, 糖尿病, 2型, 牙科刮治术, 牙周指数

Abstract:

Objective: To compare the clinical efficacy of initial periodontal therapy in periodontitis patients with or without type 2 diabetes mellitus and its correlation with white blood cell counts. Methods: In this study, 32 chronic periodontitis patients without systemic disease (CP group) and 27 chronic periodontitis patients with type 2 diabetes mellitus (CP+DM group) were enrolled. At admission, all the patients went through periodontal examination and fasting blood examination(baseline). Probing depth (PD), attachment loss (AL), bleeding index (BI), plaque index (PLI), white blood cells (WBC) counts and fasting blood glucose (FBG) were recorded respectively, while hemoglobin A1c (HbA1c) was recorded only in CP+DM group. After that, initial periodontal therapy was performed. All the tests were repeated 3 and 6 months after treatment. The changes of periodontal clinical indexes and WBC levels were compared between the two groups before and after treatment, and the correlation between WBC and periodontal clinical indexes and glucose metabolism indexes were analyzed by generalized linear mixed model. Results: At baseline, the periodontal inflammation and destruction were similar in CP and CP+DM group, but the WBC level was significantly higher in CP+DM groups [(6.01±1.26)×10⁹/L vs. (7.14±1.99)×10 ⁹/L, P=0.01]. After 3 and 6 months of initial periodontal therapy, the mean PD, AL, BI, and PLI in CP+DM and CP groups were significantly lower than the baseline, and the PD in CP+DM group was further decreased by 6 months compared with 3 months [(3.33±0.62) mm vs. (3.61±0.60) mm, P<0.05]. However, none of these periodontal indexes showed significant difference between the two groups by 3 or 6 months. In CP+DM group, HbA1c at 3 months and 6 months were significantly lower than the baseline [(7.09±0.79)% vs. (7.64±1.16)%, P<0.05; (7.06±0.78)% vs. (7.64±1.16)%, P<0.05], and FBG was significantly lower than the baseline by 6 months [(7.35±1.14) mmol/L vs. (8.40±1.43) mmol/L, P<0.05]. The WBC level in CP group was significantly lower than the baseline level by 3 months [(5.35±1.37)×10 ⁹/L vs. (6.01±1.26)×10 ⁹/L, P<0.05], while that in CP+DM group was significantly lower than the baseline level by 6 months [(6.00±1.37)×10 ⁹/L vs. (7.14±1.99)×10 ⁹/L, P<0.05]. The analysis of genera-lized linear mixed model showed that WBC level was significantly positively correlated with PD and FBG (P<0.05). Conclusion: Initial periodontal therapy can effectively improve the periodontal clinical status of patients with or without type 2 diabetes mellitus, and have benefits on glycemic control in diabetic patients. However, the response of periodontal indexes and WBC level to initial therapy were relatively delayed in diabetic patients. WBC plays an important role in the correlation between diabetes mellitus and periodontitis.

Key words: Periodontitis, Diabetes mellitus, type 2, Dental scaling, Periodontal index

中图分类号:

R781.4

徐欣然,霍芃呈,和璐,孟焕新,朱筠轩,靳东思奇. 伴与不伴糖尿病的牙周炎患者牙周基础治疗的疗效比较及其与白细胞水平的相关分析[J]. 北京大学学报（医学版）, 2022, 54(1): 48-53.

XU Xin-ran,HUO Peng-cheng,HE Lu,MENG Huan-xin,ZHU Yun-xuan,JIN Dong-si-qi. Comparison of initial periodontal therapy and its correlation with white blood cell level in periodontitis patients with or without diabetes mellitus[J]. Journal of Peking University (Health Sciences), 2022, 54(1): 48-53.

图/表 3

表1

表2

表3

参考文献 23

[1]	Graves DT, Ding Z, Yang Y. The impact of diabetes on periodontal diseases[J]. Periodontol 2000, 2020, 82(1):214-224. doi: 10.1111/prd.12318 pmid: 31850631
[2]	Genco RJ, Graziani F, Hasturk H. Effects of periodontal disease on glycemic control, complications, and incidence of diabetes mellitus[J]. Periodontol 2000, 2020, 83(1):59-65. doi: 10.1111/prd.v83.1
[3]	Costa FO, Cota LM, Lages EP, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: A 5-year follow-up study[J]. J Periodontol, 2013, 84(5):595-605. doi: 10.1902/jop.2012.120255
[4]	Mirza RE, Fang MM, Weinheimer-Haus EM, et al. Sustained inflammasome activity in macrophages impairs wound healing in type 2 diabetic humans and mice[J]. Diabetes, 2013, 63(3):1103-1114. doi: 10.2337/db13-0927
[5]	da Cruz GA, de Toledo S, Sallum EA, et al. Clinical and laboratory evaluations of non-surgical periodontal treatment in subjects with diabetes mellitus[J]. J Periodontol, 2008, 79(7):1150-1157. doi: 10.1902/jop.2008.070503
[6]	Correa F, Goncalves D, Figueredo C, et al. The short-term effectiveness of non-surgical treatment in reducing levels of interleukin-1beta and proteases in gingival crevicular fluid from patients with type 2 diabetes mellitus and chronic periodontitis[J]. J Periodontol, 2008, 79(11):2143-2150. doi: 10.1902/jop.2008.080132
[7]	Goncalves D, Correa F, Khalil NM, et al. The effect of non-surgical periodontal therapy on peroxidase activity in diabetic patients: A case-control pilot study[J]. J Clin Periodontol, 2010, 35(9):799-806. doi: 10.1111/cpe.2008.35.issue-9
[8]	Vozarova B, Weyer C, Lindsay RS, et al. High white blood cell count is associated with a worsening of insulin sensitivity and predicts the development of type 2 diabetes[J]. Diabetes, 2002, 51(2):455-461. pmid: 11812755
[9]	Zhang H, Zhen Y, Zhang W, et al. White blood cell subtypes and risk of type 2 diabetes[J]. J Diabetes Complications, 2016, 31(1):31-37. doi: 10.1016/j.jdiacomp.2016.10.029
[10]	NibaliI L, D’Aiuto F, Griffiths G, et al. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: A case-control study[J]. J Clin Periodontol, 2010, 34(11):931-937. doi: 10.1111/cpe.2007.34.issue-11
[11]	Wang X, Meng H, Xu L, et al. Mean platelet volume as an inflammatory marker in patients with severe periodontitis[J]. Platelets, 2015, 26(1):67-71. doi: 10.3109/09537104.2013.875137
[12]	Sonoki K, Nakashima S, Takata Y, et al. Decreased lipid peroxidation following periodontal therapy in type 2 diabetic patients[J]. J Periodontol, 2006, 77(11):1907-1913. pmid: 17076618
[13]	Navarro-Sanchez AB, Faria-Almeida R, Bascones-Martinez A. Effect of non-surgical periodontal therapy on clinical and immunological response and glycaemic control in type 2 diabetic patients with moderate periodontitis[J]. J Clin Periodontol, 2007, 34(10):835-843. pmid: 17850602
[14]	徐菁玲, 孟焕新, 李峥, 等. 牙周基础治疗对2型糖尿病伴慢性牙周炎患者血糖代谢指标及血清生化指标的影响[J]. 北京大学学报(医学版), 2013, 45(1):27-32.
[15]	Suvan J, Harrington Z, Petrie A, et al. Obesity as predictive factor of periodontal therapy clinical outcomes: A cohort study[J]. J Clin Periodontol, 2020, 47(5):594-601. doi: 10.1111/jcpe.13261 pmid: 31994205
[16]	Retamal I, Hernandez R, Velarde V, et al. Diabetes alters the involvement of myofibroblasts during periodontal wound healing[J]. Oral Dis, 2020, 26(5):1062-1071. doi: 10.1111/odi.v26.5
[17]	Trombelli L, Simonelli A, Franceschetti G, et al. What periodontal recall interval is supported by evidence?[J]. Periodontol 2000, 2020, 84(1):124-133. doi: 10.1111/prd.12340 pmid: 32844410
[18]	Mauri-Obradors E, Merlos A, Estrugo-Devesa A, et al. Benefits of non-surgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: A randomized controlled trial[J]. J Clin Periodontol, 2018, 45(3):345-353. doi: 10.1111/jcpe.12858 pmid: 29265454
[19]	Shiny A, Bibin YS, Shanthirani CS, et al. Association of neutrophil-lymphocyte ratio with glucose intolerance: An indicator of systemic inflammation in patients with type 2 diabetes[J]. Diabetes Technol Ther, 2014, 16(8):524-530. doi: 10.1089/dia.2013.0264
[20]	Cersosimo E, Defronzo RA. Insulin resistance and endothelial dysfunction: The road map to cardiovascular diseases[J]. Diabetes-Metab Res Rev, 2010, 22(6):423-436. doi: 10.1002/(ISSN)1520-7560
[21]	Tong PC, Lee KF, So WY, et al. White blood cell count is associated with macro- and microvascular complications in Chinese patients with type 2 diabetes[J]. Diabetes Care, 2004, 27(1):216-222. doi: 10.2337/diacare.27.1.216
[22]	Gao H, Xu J, He L, et al. Calprotectin levels in gingival crevicular fluid and serum of patients with chronic periodontitis and type 2 diabetes mellitus before and after initial periodontal therapy[J]. J Periodont Res, 2021, 56(1):121-130. doi: 10.1111/jre.v56.1
[23]	Gao H, Hou J, Meng H, et al. Proinflammatory effects and mecha-nisms of calprotectin on human gingival fibroblasts[J]. J Periodont Res, 2017, 52(6):975-983. doi: 10.1111/jre.2017.52.issue-6

相关文章 15

[1]	张培恒, 高莹, 吴红花, 张健, 张俊清. 暴发性1型糖尿病合并急性胰腺炎1例及文献回顾[J]. 北京大学学报（医学版）, 2024, 56(5): 923-927.
[2]	胡玉如,刘娟,李文静,赵亦兵,李启强,路瑞芳,孟焕新. Ⅲ期或Ⅳ期牙周炎患者龈沟液中有机酸浓度与牙周炎的关系[J]. 北京大学学报（医学版）, 2024, 56(2): 332-337.
[3]	马雨佳,卢燃藜,周泽宸,李晓怡,闫泽玉,武轶群,陈大方. 基于两样本孟德尔随机化的失眠与2型糖尿病关联研究[J]. 北京大学学报（医学版）, 2024, 56(1): 174-178.
[4]	张晗,秦亦瑄,韦帝远,韩劼. 牙周炎患者种植修复维护治疗依从性的影响因素[J]. 北京大学学报（医学版）, 2024, 56(1): 39-44.
[5]	殳畅,韩烨,孙雨哲,杨再目,侯建霞. Ⅲ期牙周炎患者牙周基础治疗前后炎症性贫血相关指标的变化[J]. 北京大学学报（医学版）, 2024, 56(1): 45-50.
[6]	鲍雷,蔡夏夏,张明远,任磊磊. 维生素D3对2型糖尿病小鼠轻度认知障碍的改善作用及机制研究[J]. 北京大学学报（医学版）, 2023, 55(4): 587-592.
[7]	裴喜燕,阳雯,欧阳翔英,孙凤. 牙周内窥镜下根面清创与牙周翻瓣术疗效比较[J]. 北京大学学报（医学版）, 2023, 55(4): 716-720.
[8]	张晓悦,林雨欣,蒋莹,张蓝超,董芒艳,池海谊,董浩宇,马利军,李智婧,常春. 自我效能在2型糖尿病患者自我管理能力和自我管理行为间的中介效应[J]. 北京大学学报（医学版）, 2023, 55(3): 450-455.
[9]	于欢,杨若彤,王斯悦,吴俊慧,王梦莹,秦雪英,吴涛,陈大方,武轶群,胡永华. 2型糖尿病患者使用二甲双胍与缺血性脑卒中发病风险的队列研究[J]. 北京大学学报（医学版）, 2023, 55(3): 456-464.
[10]	温静,欧阳翔英,裴喜燕,邱善湧,刘健如,刘文逸,曹采方. 重度牙周炎患者4年自然进展失牙的多因素分析[J]. 北京大学学报（医学版）, 2023, 55(1): 70-77.
[11]	陈阳阳,周玉博,杨静,花语蒙,原鹏波,刘爱萍,魏瑗. 双胎妊娠孕期体质量对血清高敏C反应蛋白与妊娠期糖尿病关联的影响：一项队列研究[J]. 北京大学学报（医学版）, 2022, 54(3): 427-433.
[12]	王佳敏,刘秋萍,张明露,巩超,刘舒丹,陈暐烨,沈鹏,林鸿波,高培,唐迅. 基于马尔可夫模型的社区人群糖尿病筛查预防心血管病的效果评价[J]. 北京大学学报（医学版）, 2022, 54(3): 450-457.
[13]	吴俊慧,武轶群,吴瑶,王紫荆,吴涛,秦雪英,王梦莹,王小文,王伽婷,胡永华. 北京城镇职工2型糖尿病患者缺血性脑卒中发病率及主要危险因素[J]. 北京大学学报（医学版）, 2022, 54(2): 249-254.
[14]	朱小玲,李文静,王宪娥,宋文莉,徐莉,张立,冯向辉,路瑞芳,释栋,孟焕新. 细胞色素B-245α链及胆固醇酯转运蛋白基因多态性与广泛型侵袭性牙周炎易感性的关系[J]. 北京大学学报（医学版）, 2022, 54(1): 18-22.
[15]	郜洪宇,孟焕新,侯建霞,黄宝鑫,李玮. 钙结合蛋白在健康牙周组织和实验性牙周炎组织的表达分布[J]. 北京大学学报（医学版）, 2021, 53(4): 744-749.

Metrics

Viewed

Full text

Abstract

Cited

Shared

Discussed

Items	CP group (n=32)	CP+DM group (n=27)	P
Age/years	47.16±5.35	54.22±7.87	<0.001
Male	13 (40.6)	18 (66.7)	0.046
BMI/(kg/m²)	23.48±2.11	24.25±2.26	0.182
WHR	0.88±0.06	0.88±0.03	0.614
PD/mm	4.68±0.59	4.63±0.95	0.821
AL/mm	4.43±1.20	4.56±0.99	0.669
BI	3.20±0.63	2.90±0.73	0.089
PLI	2.97±0.12	2.85±0.21	0.009
WBC/(×10⁹/L)	6.01±1.26	7.14±1.99	0.010
FBG/(mmol/L)	5.20±0.35	8.40±1.43	<0.001
HbA1c/%	-	7.64±1.16

Items	Baseline	3 months	6 months	Δ3 months	Δ6 months
PD/mm
CP group	4.68±0.59	3.62±0.64^*	3.47±0.57^*	1.07±0.63	1.20±0.68
CP+DM group	4.63±0.95	3.61±0.60^*	3.33±0.62^*§	1.02±0.86	1.30±0.84
AL/mm
CP group	4.43±1.20	3.87±1.07^*	3.58±0.81^*§	0.56±0.66	0.85±0.66
CP+DM group	4.56±0.99	3.79±0.83^*	3.76±0.86^*	0.77±0.85	0.80±0.62
BI
CP group	3.20±0.63	2.09±0.61^*	2.03±0.55^*	1.12±0.82	1.18±0.82
CP+DM group	2.90±0.73	1.97±0.56^*	1.84±0.42^*	0.93±0.85	1.06±0.68
PLI
CP group	3.00±0.22	2.59±0.57^*	1.85±0.75^*§	0.41±0.52	1.15±0.73
CP+DM group	2.85±0.21^#	2.42±0.58^*	2.03±0.65^*§	0.43±0.52	0.81±0.65
WBC/(×10⁹/L)
CP group	6.01±1.26	5.35±1.37^*	5.51±1.51	0.66±1.11	0.50±1.18
CP+DM group	7.14±1.99^#	6.57±1.68	6.00±1.37^*	0.57±2.20	1.14±1.80
FBG/(mmol/L)
CP group	5.20±0.35	5.20±0.32	5.33±0.42	0.00±0.31	-0.13±0.47
CP+DM group	8.40±1.43^#	7.72±1.40^#	7.35±1.14^*#	0.68±1.52^#	1.05±1.59^#
HbA1c/%
CP group	-	-	-	-	-
CP+DM group	7.64±1.16	7.09±0.79^*	7.06±0.78^*	0.55±0.78	0.58±0.83

Parameter	β	SE	t/Z	P	95%CI
Model 1
Intercept	3.19	0.77	4.12	<0.001	1.66 to 4.71
PD	0.57	0.22	2.56	0.011	0.13 to 1.00
FBG	0.28	0.09	3.25	0.001	0.11 to 0.45
Model 2
Intercept	3.37	0.99	3.39	0.001	1.41 to 5.33
PD	0.55	0.22	2.48	0.014	0.11 to 0.99
FBG	0.27	0.09	2.98	0.003	0.09 to 0.44
Model 3
Intercept	4.10	2.34	1.75	0.082	-0.52 to 8.72
PD	0.53	0.22	2.36	0.019	0.09 to 0.96
FBG	0.29	0.09	3.33	0.001	0.12 to 0.46
Model 4
Intercept	4.73	2.47	1.91	0.058	-0.16 to 9.61
PD	0.45	0.23	1.98	0.050	0.001 to 0.90
FBG	0.26	0.09	2.94	0.004	0.09 to 0.44