Journal of Peking University (Health Sciences) ›› 2024, Vol. 56 ›› Issue (1): 45-50. doi: 10.19723/j.issn.1671-167X.2024.01.008

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Changes of parameters associated with anemia of inflammation in patients with stage Ⅲ periodontitis before and after periodontal initial therapy

Chang SHU,Ye HAN,Yuzhe SUN,Zaimu YANG,Jianxia HOU*()   

  1. Department of Periodontology, Peking University School and Hospital of Stomatology & National Center for Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices & Beijing Key Laboratory of Digital Stomatology, Beijing 100081, China
  • Received:2023-10-11 Online:2024-02-18 Published:2024-02-06
  • Contact: Jianxia HOU E-mail:jxhou@163.com
  • Supported by:
    the National Natural Science Foundation of China(82071117);the Beijing Natural Science Foundation(7212136)

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Abstract:

Objective: To investigate the differences and similarities of parameters associated with anemia of inflammation between patients with stage Ⅲ periodontitis and periodontally healthy volunteers, and to explore the influence of periodontal initial therapy on those indicators. Methods: Patients with stage Ⅲ periodontitis and periodontally healthy volunteers seeking periodontal treatment or prophylaxis at Department of Periodontology, Peking University School and Hospital of Stomatology from February 2020 to February 2023 were enrolled. Their demographic characteristics, periodontal parameters (including probing depth, clinical attachment loss, bleeding index), and fasting blood were gathered before periodontal initial therapy. Three months after periodontal initial therapy, the periodontal parameters of the patients with stage Ⅲ periodontitis were re-evaluated and their fasting blood was collected again. Blood routine examinations (including white blood cells, red blood cells, hemoglobin, packed cell volume, mean corpuscular volume of erythrocytes, and mean corpuscular hemoglobin concentration) were performed. And ferritin, hepcidin, erythropoietin (EPO) were detected with enzyme-linked immunosorbent assay (ELISA). All data analysis was done with SPSS 21.0, independent sample t test, paired t test, and analysis of covariance were used for comparison between the groups. Results: A total of 25 patients with stage Ⅲ periodontitis and 25 periodontally healthy volunteers were included in this study. The patients with stage Ⅲ periodontitis were significantly older than those in periodontally healthy status [(36.72±7.64) years vs. (31.44±7.52) years, P=0.017]. The patients with stage Ⅲ periodontitis showed lower serum hemoglobin [(134.92±12.71) g/L vs. (146.52±12.51) g/L, P=0.002] and higher serum ferritin [(225.08±103.36) μg/L vs. (155.19±115.38) μg/L, P=0.029], EPO [(41.28±12.58) IU/L vs. (28.38±10.52) IU/L, P < 0.001], and hepcidin [(48.03±34.44) μg/L vs. (27.42±15.00) μg/L, P=0.009] compared with periodontally healthy volunteers. After adjusting the age with the covariance analysis, these parameters (hemoglobin, ferritin, EPO, and hepcidin) showed the same trends as independent-sample t test with statistical significance. Three months after periodontal initial therapy, all the periodontal parameters showed statistically significant improvement. The serum hemoglobin raised [(146.05±15.48) g/L vs. (133.77± 13.15) g/L, P < 0.001], while the serum ferritin [(128.52±90.95) μg/L vs. (221.22±102.15) μg/L, P < 0.001], EPO [(27.66±19.67) IU/L vs. (39.63± 12.48) IU/L, P=0.004], and hepcidin [(32.54±18.67) μg/L vs. (48.18±36.74) μg/L, P=0.033] decreased compared with baseline. Conclusion: Tendency of iron metabolism disorder and anemia of inflammation was observed in patients with stage Ⅲ periodontitis, which can be attenuated by periodontal initial therapy.

Key words: Periodontitis, Anemia of inflammation, Iron metabolism, Periodontal diseases

CLC Number: 

  • R781.4

Table 1

Demographics of participants"

Items Control Stage Ⅲ periodontitis P
Age/years, ${\bar x}$±s 31.44±7.52 36.72±7.64 0.017
Gender, n
  Male 13 14 0.777
  Female 12 11
PD/mm, ${\bar x}$±s 1.56±0.68 4.71±0.95 < 0.001
BI, ${\bar x}$±s 1.12±0.52 3.44±0.57 < 0.001
CAL/mm, ${\bar x}$±s 0 4.27±0.98 < 0.001

Table 2

Fasting blood examinations of patients with stage Ⅲ periodontitis and periodontally healthy volunteers"

Items Control, ${\bar x}$±s Stage Ⅲ periodontitis, ${\bar x}$±s P
WBC/(×109/L) 5.90±1.13 6.48±1.74 0.169
RBC/(×1012/L) 4.85±0.45 4.86±0.56 0.962
HGB/(g/L) 146.52±12.51 134.92±12.71 0.002**
HCT 0.43±0.04 0.42±0.04 0.382
MCV/fL 89.24±3.75 87.62±5.81 0.246
MCH/(pg/cell) 29.86±1.56 29.68±2.67 0.763
MCHC/(g/dL) 334.52±10.35 338.2±13.56 0.286
Transferrin/(mg/dL) 268.81±37.86 254.92±47.25 0.254
Ferritin/(μg/L) 155.19±115.38 225.08±103.36 0.029*
Hepcidin/(μg/L) 27.42±15.00 48.03±34.44 0.009**
EPO/(IU/L) 28.38±10.52 41.28±12.58 < 0.001***

Table 3

Analysis of covariance of fasting blood examinations of patients with stage Ⅲ periodontitis and periodontally healthy volunteers"

Items Control, ${\bar x}$±s Stage Ⅲ periodontitis, ${\bar x}$±s P
WBC/(×109/L) 5.79±0.30 6.59±0.30 0.070
RBC/(×1012/L) 4.84±0.11 4.87±0.11 0.811
HGB/(g/L) 146.51±2.63 134.93±2.63 0.004**
HCT 0.43±0.01 0.43±0.01 0.627
MCV/fL 89.08±1.02 87.79±1.02 0.386
MCH/(pg/cell) 29.86±0.46 29.68±0.46 0.784
MCHC/(g/dL) 335.18±2.48 337.54±2.48 0.518
Transferrin/(mg/dL) 269.48±8.92 254.36±8.92 0.250
Ferritin/(μg/L) 152.01±22.75 228.26±22.75 0.026*
Hepcidin/(μg/L) 27.33±5.54 48.13±5.54 0.013*
EPO/(IU/L) 28.64±2.41 41.02±2.41 0.001**

Table 4

Periodontal clinical parameters pre- and post-treatment"

Items Baseline, ${\bar x}$±s After therapy, ${\bar x}$±s P
PD/mm 4.66±0.88 2.92±0.45 < 0.001
BI 3.46±0.57 1.66±0.74 < 0.001
CAL/mm 4.23±0.89 3.03±0.75 < 0.001

Table 5

Fasting blood parameters pre- and post-treatment of stage Ⅲ periodontitis"

Items Baseline, ${\bar x}$±s After therapy, ${\bar x}$±s P
WBC/(×109/L) 6.43±1.83 6.28±1.88 0.401
RBC/(×1012/L) 4.85±0.60 4.79±0.56 0.272
HGB/(g/L) 133.77±13.15 146.05±15.48 < 0.001***
HCT 0.42±0.04 0.42±0.04 0.244
MCV/fL 87.40±6.14 87.27±6.19 0.655
MCH/(pg/cell) 29.64±2.83 29.31±2.60 0.051
MCHC/(g/dL) 338.55±14.33 335.18±12.12 0.102
Transferrin/(mg/dL) 257.45±49.62 258.06±34.06 0.957
Ferritin/(μg/L) 221.22±102.15 128.52±90.95 < 0.001***
Hepcidin/(μg/L) 48.18±36.74 32.54±18.67 0.033*
EPO/(IU/L) 39.63±12.48 27.66±19.67 0.004**
1 Lu HX , Tao DY , Lo ECM , et al. The 4th National Oral Health Survey in the mainland of China: Background and methodology[J]. Chin J Dent Res, 2018, 21 (3): 161- 165.
2 Tonetti MS , Greenwell H , Kornman KS . Staging and grading of periodontitis: Framework and proposal of a new classification and case definition[J]. J Periodontol, 2018, 89 (Suppl 1): S159- S172.
3 Jiao J , Jing W , Si Y , et al. The prevalence and severity of periodontal disease in mainland China: Data from the Fourth National Oral Health Survey (2015-2016)[J]. J Clin Periodontol, 2021, 48 (2): 168- 179.
doi: 10.1111/jcpe.13396
4 Guo LN , Yang YZ , Feng YZ . Serum and salivary ferritin and hepcidin levels in patients with chronic periodontitis and type 2 diabetes mellitus[J]. BMC Oral Health, 2018, 18 (1): 63.
doi: 10.1186/s12903-018-0524-4
5 Zheng X , Li X , Zhen J , et al. Periodontitis is associated with stroke[J]. J Transl Med, 2023, 21 (1): 697.
doi: 10.1186/s12967-023-04545-1
6 Gonzalez DA, Bianchi ML, Armada M, et al. Hyposalivation and periodontal disease as oral non-articular characteristics in rheumatoid arthritis [J/OL]. Clin Rheumatol, 2023, doi: 10.1007/s10067-023-06718-1. Online ahead of print. https://link.sprin-ger.com/article/10.1007/s10067-023-06718-1.
7 AlSharief M , Alabdurubalnabi E . Periodontal pathogens and adverse pregnancy outcomes: A narrative review[J]. Life (Basel), 2023, 13 (7): 1559.
8 Shi T , Wang J , Dong J , et al. Periodontopathogens Porphyromonas gingivalis and Fusobacterium nucleatum and their roles in the progression of respiratory diseases[J]. Pathogens, 2023, 12 (9): 1110.
doi: 10.3390/pathogens12091110
9 Zhao C , Kuraji R , Ye C , et al. Nisin a probiotic bacteriocin mitigates brain microbiome dysbiosis and Alzheimer' s disease-like neuroinflammation triggered by periodontal disease[J]. J Neuroinflammation, 2023, 20 (1): 228.
doi: 10.1186/s12974-023-02915-6
10 Beukers N , Su N , van der Heijden G , et al. Periodontitis is associated with multimorbidity in a large dental school population[J]. J Clin Periodontol, 2023, 50 (12): 1621- 1632.
doi: 10.1111/jcpe.13870
11 Ganz T . Anemia of inflammation[J]. N Engl J Med, 2019, 381 (12): 1148- 1157.
doi: 10.1056/NEJMra1804281
12 Thomas C , Thomas L . Biochemical markers and hematologic indices in the diagnosis of functional iron deficiency[J]. Clin Chem, 2002, 48 (7): 1066- 1076.
doi: 10.1093/clinchem/48.7.1066
13 Handelman GJ , Levin NW . Iron and anemia in human biology: A review of mechanisms[J]. Heart Fail Rev, 2008, 13 (4): 393- 404.
doi: 10.1007/s10741-008-9086-x
14 张梦雪, 王小钦. 铁稳态失调相关的炎症性贫血发病机制及诊断进展[J]. 诊断学理论与实践, 2018, 17 (5): 601- 605.
15 de Las Cuevas Allende R , Díaz de Entresotos L , Conde Díez S . Anaemia of chronic diseases: Pathophysiology, diagnosis and treatment[J]. Med Clin (Barc), 2021, 156 (5): 235- 242.
doi: 10.1016/j.medcli.2020.07.035
16 Hutter JW , van der Velden U , Varoufaki A , et al. Lower numbers of erythrocytes and lower levels of hemoglobin in periodontitis patients compared to control subjects[J]. J Clin Periodontol, 2001, 28 (10): 930- 936.
doi: 10.1034/j.1600-051x.2001.028010930.x
17 郜洪宇, 徐菁玲, 孟焕新, 等. 牙周基础治疗对2型糖尿病伴慢性牙周炎患者红细胞、血小板相关指标的影响[J]. 北京大学学报(医学版), 2020, 52 (4): 750- 754.
18 Nibali L , Darbar U , Rakmanee T , et al. Anemia of inflammation associated with periodontitis: Analysis of two clinical studies[J]. J Periodontol, 2019, 90 (11): 1252- 1259.
doi: 10.1002/JPER.19-0124
19 Kolte RA , Kolte AP , Deshpande NM . Assessment and comparison of anemia of chronic disease in healthy subjects and chronic periodontitis patients: A clinical and hematological study[J]. J Indian Soc Periodontol, 2014, 18 (2): 183- 186.
doi: 10.4103/0972-124X.131321
20 Pradeep AR , Anuj S . Anemia of chronic disease and chronic periodontitis: Does periodontal therapy have an effect on anemic status?[J]. J Periodontol, 2011, 82 (3): 388- 394.
doi: 10.1902/jop.2010.100336
21 Han Y , Huang W , Meng H , et al. Pro-inflammatory cytokine interleukin-6-induced hepcidin, a key mediator of periodontitis-related anemia of inflammation[J]. J Periodontal Res, 2021, 56 (4): 690- 701.
doi: 10.1111/jre.12865
22 Han Y , Luo Z , Yue ZG , et al. The tendency of anemia of inflammation in periodontal diseases[J]. Clin Sci (Lond), 2023, 137 (3): 251- 264.
doi: 10.1042/CS20220524
23 Patel MD , Shakir QJ , Shetty A . Interrelationship between chronic periodontitis and anemia: A 6-month follow-up study[J]. J Indian Soc Periodontol, 2014, 18 (1): 19- 25.
doi: 10.4103/0972-124X.128194
24 Massey AC . Microcytic anemia. Differential diagnosis and management of iron deficiency anemia[J]. Med Clin North Am, 1992, 76 (3): 549- 566.
doi: 10.1016/S0025-7125(16)30339-X
25 Weiss G , Ganz T , Goodnough LT . Anemia of inflammation[J]. Blood, 2019, 133 (1): 40- 50.
doi: 10.1182/blood-2018-06-856500
26 Chakraborty S , Tewari S , Sharma RK , et al. Effect of non-surgical periodontal therapy on serum ferritin levels: An interventional study[J]. J Periodontol, 2014, 85 (5): 688- 696.
doi: 10.1902/jop.2013.130107
27 Ong DS , Wang L , Zhu Y , et al. The response of ferritin to LPS and acute phase of Pseudomonas infection[J]. J Endotoxin Res, 2005, 11 (5): 267- 280.
doi: 10.1177/09680519050110050301
28 Huang W , Zhan Y , Zheng Y , et al. Up-regulated ferritin in periodontitis promotes inflammatory cytokine expression in human periodontal ligament cells through transferrin receptor via ERK/P38 MAPK pathways[J]. Clin Sci (Lond), 2019, 133 (1): 135- 148.
doi: 10.1042/CS20180679
29 Johnston PA , Grandis JR . STAT3 signaling: Anticancer strategies and challenges[J]. Mol Interv, 2011, 11 (1): 18- 26.
doi: 10.1124/mi.11.1.4
30 Drakesmith H , Prentice AM . Hepcidin and the iron-infection axis[J]. Science, 2012, 338 (6108): 768- 772.
doi: 10.1126/science.1224577
31 Malyszko J , Malyszko JS , Matuszkiewicz-Rowinska J . Hepcidin as a therapeutic target for anemia and inflammation associated with chronic kidney disease[J]. Expert Opin Ther Targets, 2019, 23 (5): 407- 421.
doi: 10.1080/14728222.2019.1599358
32 Arndt S , Maegdefrau U , Dorn C , et al. Iron-induced expression of bone morphogenic protein 6 in intestinal cells is the main regulator of hepatic hepcidin expression in vivo[J]. Gastroenterology, 2010, 138 (1): 372- 382.
33 Kautz L , Jung G , Du X , et al. Erythroferrone contributes to hepcidin suppression and iron overload in a mouse model of beta-thalassemia[J]. Blood, 2015, 126 (17): 2031- 2037.
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