Vitamin C in plasma and leucocytes in relation to periodontitis
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J Clin Periodontol 2012; 39: 905–912 doi: 10.1111/j.1600-051X.2012.01927.x
Vitamin C in plasma and Denica Kuzmanova, Ineke D. C.
Jansen, Ton Schoenmaker, Kamran
Nazmi, Wijnand J. Teeuw, Sergio Biz-
leucocytes in relation to zarro, Bruno G. Loos and
Ubele van der Velden
Department of Periodontology and Oral
periodontitis Biochemistry, Academic Centre for Dentistry
Amsterdam (ACTA), University of Amsterdam
and VU University Amsterdam, The
Netherlands
Kuzmanova D, Jansen IDC, Schoenmaker T, Nazmi K, Teeuw WJ, Bizzarro S,
Loos BG, Velden van der U. Vitamin C in plasma and leucocytes in relation to
periodontitis. J Clin Periodontol 2012; 39: 905–912. doi: 10.1111/j.1600-
051X.2012.01927.x.
Abstract
Aim: To test the hypothesis that vitamin C concentrations in plasma, polymor-
phonuclear neutrophilic leucocytes (PMNs) and peripheral blood mononuclear
cells (PBMCs) are lower in periodontitis patients compared with healthy controls.
Methods: Twenty-one untreated periodontal patients and 21 healthy controls
matched for age, gender, race and smoking habits were selected. Dietary vitamin
C intake was assessed by a self-administered dietary record. Fasting blood sam-
ples were obtained and analysed for vitamin C concentrations in plasma, PMNs
and PBMCs by means of high-pressure liquid chromatography (HPLC).
Results: Plasma vitamin C was lower in periodontitis patients compared with con-
trols (8.3 and 11.3 mg/l, respectively, p = 0.03). Only in the control group a posi-
tive correlation was present between vitamin C intake and plasma values. No
differences could be assessed between patients and controls regarding vitamin C
dietary intake and levels in PMNs and PBMCs. In the patient group, pocket depth
appeared to be negatively associated with the vitamin C concentration in PMNs.
Conclusion: Although the relationship between low plasma vitamin C levels and Key words: leucocytes; periodontitis; plasma;
periodontitis is clear, the disease cannot be explained by insufficient vitamin C vitamin C
storage capacity of leucocytes; the question remains through which mechanism
low plasma vitamin C levels are related to periodontitis. Accepted for publication 19 June 2012
For many years vitamin C (ascorbic role in periodontal health which is Matthews 2007). Both ROS and
acid) has been recognized to play a supported by an inverse association immune cells are implicated in the
between serum/plasma vitamin C pathophysiology of periodontitis
concentrations and periodontitis (Kornman et al. 1997). It is known
Conflict of interest and source of
(Amarasena et al. 2005, Panjamur- that leucocytes, in particular poly-
funding statement
thy et al. 2005, Staudte et al. 2005, morphonuclear neutrophilic leuco-
The authors declare that they have no Amaliya et al. 2007, Chapple et al. cytes (PMNs) and mononuclear cells
conflicts of interest. 2007). During the last decades there (MNs), have a marked ability to
The study was self funded by the is growing evidence for the impor- concentrate ascorbic acid (Evans
authors and their Institution. The tance of vitamin C as antioxidant et al. 1982). The storage of vitamin
department of periodontology is funded against reactive oxygen species C has been attributed to increased
in part by a grant from the University
(ROS) and in leucocyte function in needs of these cells for the vitamin
of Amsterdam for the focal point “Oral
healthy as well as periodontally and suggests that it plays a signifi-
infection and inflammation”.
diseased subjects (Chapple & cant role in normal cell function
© 2012 John Wiley & Sons A/S 905906 Kuzmanova et al.
(Boxer et al. 1979, Wolf 1993). root length at 1 tooth per quad- participants were asked to fill in
Vitamin C aids in the bactericidal rant and 20 teeth. An equal num- what they consumed 3 days prior to
activity of PMNs and monocytes/ ber of controls matched for age, the examination and to answer ques-
macrophages, providing enhanced gender, race and smoking status tions about their dietary habits as
synthesis of nitric oxide (Sharma were recruited if they presented with well as the use of food supplements.
et al. 2003, 2004). It increases the 20 teeth and a distance between The reported number of servings
chemotactic responsiveness of the cemento-enamel junction and the was obtained. Using the Netherlands
peripheral blood leucocytes and inter-dental alveolar bone crest of Food Composition Tables (Neder-
promotes the assembly of cellular 3 mm on dental radiographs not landse Voedingsmiddelentabel 2006)
microtubules involved in providing a older than 12 months. Radiographic the different food and beverage items
structural framework for the cell evaluation of bone levels was per- consumed were categorized as high,
(Boxer et al. 1979). In MNs, vitamin formed using a light box and a Shei fair, low or no vitamin C when they
C has been suggested to increase glu- ruler, scoring bone loss in categories provided >60 mg, 31–60 mg, 2–
tathione (Lenton et al. 2003), to of 10% increments relative to the 30 mg and 1/3 of the administered dietary record. All method using a commercial medium
© 2012 John Wiley & Sons A/SVitamin C in periodontitis 907
(Axis-Shield PoC AS, Lympho- wavelength 245 nm. Cellular content analyses, p < 0.05 values were con-
prepTM, Oslo, Norway). Briefly, of vitamin C is expressed as lg/108 sidered statistically significant.
whole blood was diluted 1:1 with cells and plasma concentrations as
phosphate buffered saline (PBS) plus mg/l. Plasma vitamin C levels were
Results
1% citrate before being carefully described as deficient (908 Kuzmanova et al.
Table 1. General characteristics of the study population. Values represent numbers (%) of hand and the predictors on the other
subjects or means ± SD are presented in Table 4. In the
Background Control Periodontitis control group a significant positive
characteristics subjects (N = 21) patients (N = 21) correlation was present between
plasma levels and the total intake of
Age (years) 46.4 ± 9.0 46.9 ± 10.8 vitamin C. In contrast, in the patient
Gender group none of the predictors showed
Male 10 (48%) 10 (48%)
a significant relationship with the
Female 11 (52%) 11 (52%)
Ethnicity
plasma vitamin C values. For PMNs,
Non-Caucasian 4 (19%) 4 (19%) only in the patient group a significant
Caucasian 17 (81%) 17 (81%) result was found i.e. PPD was nega-
Smoking tively correlated with vitamin C in
Non-smoker 10 (48%) 10 (48%) PMNs. For PBMCs, in the control
Smoker 11 (52%) 11 (52%) group a negative correlation was
Pack-year 20.1 ± 11.8 20.2 ± 13.8 found with smoking, i.e. non-smokers
Education had higher vitamin C concentration
50%: 54% versus 11%
Periodontitis respectively (p = 0.001). Both were
Control (N = 21) (N = 21) p-value smokers and showed vitamin C
depletion i.e. the lowest plasma
No. servings >31 mg/100 mg vitamin C 1.9 ± 2.0 1.1 ± 1.3 0.12 vitamin C values of all subjects of
2–30 mg/100 mg vitamin C 10.2 ± 6.4 9.5 ± 4.1 0.68 the study population: 2.4 andVitamin C in periodontitis 909
Table 3. Vitamin C intake and vitamin C concentrations in plasma, PMNs and PBMCs for are comparable to figures from con-
controls (N = 21) and periodontitis patients (N = 21) in relation to gender (11 females), and trols in case-control studies of the
smoking (10 non-smokers). Values are means (±SD) medical literature which range from
Control Periodontitis p-value 11.5 mg/l to 13.4 mg/l (Göçmen et al.
2008, Hengstermann et al. 2008,
Total intake vitamin C Braga et al. 2011, Chen et al. 2011,
Gender Males 9.9 ± 7.8 10.6 ± 5.3 0.82 Zanon-Moreno et al. 2011). In the
Females 18.6 ± 9.8 14.0 ± 6.0 0.21
periodontitis group of our study the
p-value 0.037 0.20
Smoking Non-smokers 18.3 ± 10.7 13.3 ± 6.3 0.22
mean plasma vitamin C level
Smokers 11.0 ± 7.7 11.3 ± 5.3 0.92 amounted to 8.3 ± 3.9 mg/l. This
p-value 0.087 0.45 value is in accordance with data from
studies where vitamin C in plasma/
Vitamin C in plasma (mg/l) serum was measured in periodontitis
Gender Males 9.1 ± 3.4 8.2 ± 3.8 0.58
patients using HPLC: 7.9 ± 5.4 mg/l
Females 12.6 ± 3.2 8.4 ± 3.9 0.012
p-value 0.025 0.90
(Amaliya et al. 2007) and 7.2 mg/l
Smoking Non-smokers 11.6 ± 3.1 9.1 ± 2.6 0.067 (range 0.2–22.6 mg/l) (Amarasena
Smokers 10.4 ± 4.2 7.6 ± 4.6 0.16 et al. 2005).
p-value 0.48 0.39 The results of the multiple regres-
sion analysis showed that in the
Vitamin C in PMNs (lg/108 cells)
control group a highly significant
Gender Males 51.8 ± 13.0 55.2 ± 20.1 0.66
Females 55.3 ± 16.5 67.9 ± 21.0* 0.16
correlation existed between the
p-value 0.60 0.20 plasma vitamin C values and the
Smoking Non-smokers 56.6 ± 17.9 70.9 ± 22.7† 0.14 total vitamin C intake whereas such
Smokers 50.9 ± 11.2 53.9 ± 19.2 0.66 a relationship was not present in the
p-value 0.39 0.087 patient group. The finding that in
disease, the vitamin C intake does
Vitamin C in PBMCs (lg/108 cells)
Gender Males 85.9 ± 14.0 100.3 ± 39.3 0.29
not correspond to plasma vitamin C
Females 95.5 ± 24.6 100.9 ± 62.5* 0.79 levels is not a new observation. For
p-value 0.29 0.98 example, it has been shown that in
Smoking Non-smokers 100.9 ± 23.8 96.2 ± 59.0† 0.81 Helicobacter pylori infections, the
Smokers 81.8 ± 11.3 104.2 ± 45.7 0.13 plasma vitamin C levels are lower
p-value 0.027 0.74 than expected on the basis of the
vitamin C intake (Woodward et al.
*N = 10.
†
N = 9. 2001). This could be explained by an
increased turnover of vitamin C due
Table 4. Relationship between vitamin C intake, subjects characteristics and vitamin C con- to ROS generated by the inflamma-
centrations in plasma, PMNs and PBMCs. Results of regression analyses of predictor vari- tory response. It has been shown
ables that showed significant correlations that low vitamin C plasma values
Predictor variables b (95% CI) Explained variance p-value are related to disease conditions that
are thought to be caused or exacer-
Vitamin C concentration in plasma bated by oxidative stress. However,
Controls Total intake vitamin C 0.62 (0.94, 0.38) 38.4% 0.002 it is not clear whether low plasma
Gender n.r. – – and tissue vitamin C levels either
Patients No predictors to enter – – – contribute to each of these diseases
into the model
or are a consequence of the disease
Vitamin C concentration in PMNs process or merely associated with the
Controls No predictors to enter – – – disease condition (Padayatty et al.
into the model 2003). Another explanation for the
Patients Pocket depth (mm) 0.47 ( 30.30, 0.90) 22.1% 0.039 absence of a positive correlation
Bleeding on probing n.r. – – between vitamin C intake and
Vitamin C concentration in PBMCs plasma vitamin C values in peri-
Controls Smoking* 0.48 ( 35.91, 2.38) 23.0% 0.027 odontal patients may be a different
Patients Age 0.47 (0.15, 4.99) 22.1% 0.039 genetic make-up. Vitamin C can be
Education n.r. – – actively transported across mem-
*Non-smokers have higher vitamin C concentrations than smokers. branes against its concentration gra-
n.r.: not retained in the model. dient by two sodium-dependent
vitamin C transporter proteins
stores of vitamin C in leucocytes to are associated with periodontitis (Stratakis et al. 2000) encoded by
explain a possible mechanism of this (Melnick et al. 1988, Panjamurthy two separate genes and for both
micronutrient in the pathogenesis of et al. 2005, Staudte et al. 2005, genetic polymorphisms have been
periodontitis. The present findings Thomas et al. 2010). The mean demonstrated (Eck et al. 2004). In a
confirm previous results that lower plasma vitamin C levels of the con- recent study, it was confirmed that
plasma vitamin C concentrations trols in the present study (11.3 mg/l) genetic variation in vitamin C trans-
© 2012 John Wiley & Sons A/S910 Kuzmanova et al.
Table 5. Background and dental characteristics (mean ± SD) of vitamin C depleted and non- be suggested that this compromised
depleted periodontitis patients. Values represent numbers (%) of subjects or means ± SD status could be due to a reduced con-
Patients by vitamin C group centration of vitamin C in the PMNs
of the crevicular fluid. These PMNs
Depleted (N = 4) Non-depleted (N = 17) p-value with possibly low intracellular
vitamin C stores do not return into
Background characteristics the blood circulation but are leaving
Age (years) 44.5 ± 3.9 47.5 ± 11.8 0.63 the tissues into the oral cavity. It has
Gender (males) 2 (50%) 8 (47%) 1.00
been estimated that the number of
Ethnicity (Caucasians) 4 (100%) 13 (77%) 0.55
Smoking (smokers) 4 (100%) 7 (41%) 0.09
leucocytes leaving the body in this
Education (Vitamin C in periodontitis 911
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© 2012 John Wiley & Sons A/S912 Kuzmanova et al.
Clinical Relevance Principal findings: Vitamin C intake Practical implications: Although the
Scientific rationale for the study: and vitamin C concentrations in relationship between low plasma
During the last decades it became PMNs and PBMCs were not vitamin C concentrations and peri-
evident that periodontitis is associ- different between patients and con- odontitis could not be explained by
ated with low plasma vitamin C trols. However, plasma vitamin C a hampered leucocyte function due
levels. There is also growing was reduced in periodontitis patients to a lack of intracellular vitamin C,
evidence for the importance of compared with controls. The positive it seems justified that in periodon-
vitamin C for leucocyte function relationship between vitamin C tal practice more attention is paid
and as antioxidant against reactive intake and plasma concentration in to the diet of patients in relation to
oxygen species (ROS) in periodon- controls was not present in vitamin C.
titis. However, there are currently periodontitis patients. In periodonti-
no data available of vitamin C tis, increasing probing pocket depth
concentrations in PMNs and was correlated with decreasing
PBMCs of periodontitis patients. vitamin C concentrations in PMNs.
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