original papers - Advances in Clinical and Experimental Medicine

ORIGINAL PAPERS
Adv Clin Exp Med 2007, 16, 6, 743–749
ISSN 1230−025X
© Copyright by Silesian Piasts
University of Medicine in Wrocław
AGNIESZKA JAWOROWSKA1, GRZEGORZ BAZYLAK1, EUGENIA GOSPODAREK2
Seropositivity for Chlamydophila pneumoniae
is Associated with Increased Body Mass Index
and Serum Lipid Levels: Evidence from the Sample
Urban Population in Bydgoszcz*
Wpływ zakażeń Chlamydophila pneumoniae na wskaźniki otyłości
i gospodarki lipidowej u osób dorosłych z terenu Bydgoszczy
1
Department of Bromatology and Molecular Nutrition, Faculty of Pharmacy, Collegium Medicum,
Nicolaus Copernicus University, Bydgoszcz, Poland
2
Department of Microbiology, Faculty of Pharmacy, Collegium Medicum, Nicolaus Copernicus University,
Bydgoszcz, Poland
Abstract
Background. Although it is well known that obesity is a multifactoral disease, the possibility that some viruses or
bacteria might be a serious etiologic factor in this metabolic disorder has received relatively little attention.
Objectives. As no information is available on a link between Chlamydophila pneumoniae infections and the pre−
valence of obesity in Poland, this study was conducted to provide such pilot data from a sample of professionally
active adults randomly recruited from an urban area in Bydgoszcz.
Material and Methods. Anthropometric measurements were obtained from 39 healthy middle−aged adult subjects
(4 male, 35 female) of whom 27 were obese or overweight. Antibody status (IgG, IgA, IgM) was determined by
enzyme−linked immunosorbent assay (ELISA). The total cholesterol (TChol) and triglyceride (TG) concentrations
in serum were performed by standard enzymatic methods.
Results. The group of subjects with IgG antibodies for C. pneumoniae was characterized by higher BMI (31.4 ± 5.5
vs. 27.4 ± 6.3 kg/m2, p = 0.038), higher serum TChol (5.64 ± 0.91 vs. 5.02 ± 0.81 mmol/l, p = 0.047), and higher
TG level (1.38 ± 0.34 vs. 1.16 ± 0.49 mmol/l, p = 0.047) than seronegative subjects. Seropositivity for C. pneumo−
niae IgA antibodies was associated with higher serum TChol concentration (5.91 ± 0.67 vs. 5.15 ± 0.93 mmol/l,
p = 0.007). No subjects were positive for IgM antibodies.
Conclusions. The results of this pilot study indicate that C. pneumoniae infection is associated with higher body
mass index and elevated serum lipid concentrations in a sample of a middle−aged adult urban population from Byd−
goszcz (Adv Clin Exp Med 2007, 16, 6, 743–749).
Key words: Chlamydophila pneumoniae, infectobesity, BMI, serum cholesterol, serum triglycerides.
Streszczenie
Wprowadzenie. Otyłość jest jednostką chorobową o złożonym i wieloczynnikowym podłożu, możliwość jednak
udziału czynnika infekcyjnego w etiologii otyłości była rzadko rozważana, a w Polsce nie podejmowano dotych−
czas tego problemu.
Cel pracy. Określenie współzależności między obecnością w surowicy przeciwciał swoistych dla Chlamydophila
pneumoniae a występowaniem otyłości i gospodarką lipidową aktywnych zawodowo osób dorosłych stanowiących
próbkę populacji wielkomiejskiej z terenu Bydgoszczy.
Materiał i metody. W grupie 39 dorosłych osób w średnim wieku (w tym 27 z nadwagą lub otyłością) objętych
badaniami przeprowadzono pomiary antropometryczne. Stężenie cholesterolu całkowitego (TChol) i triglicerydów
(TG) w surowicy badanych osób oceniono z zastosowaniem metody enzymatycznej. Do oznaczenia obecności
przeciwciał klasy IgG, IgA, IgM dla C. pneumoniae wykorzystano metodę immunoenzymatyczną.
* The research was supported by grant no. BW−68−2006.
744
A. JAWOROWSKA, G. BAZYLAK, E. GOSPODAREK
Wyniki. Odnotowano, że osoby ze stwierdzoną obecnością przeciwciał klasy IgG charakteryzowały się statystycz−
nie istotnie wyższym BMI (31,4 ± 5,5 vs. 27,4 ± 6,3 kg/m2; p = 0,038) oraz stężeniem TChol (5,64 ± 0,91 vs. 5,02 ±
± 0,81 mmol/l; p = 0,047) i TG (1,38 ± 0,34 vs. 1,16 ± 0,49 mmol/l; p = 0,047) w surowicy niż osoby seronega−
tywne. Wykazano również, że obecność w surowicy przeciwciał klasy IgA jest związana z istotnie większym stę−
żeniem TChol (5,91 ± 0,67 vs. 5,15 ± 0,93 mmol/l; p = 0.007). Nie stwierdzono obecności przeciwciał klasy IgM
w badanej grupie osób z terenu Bydgoszczy.
Wnioski. Uzyskane wstępne wyniki wskazują na duże prawdopodobieństwo udziału czynnika infekcyjnego
w etiologii nadwagi i otyłości. Wykazano również współzależność między obecnością przeciwciał swoistych dla
C. pneumoniae a profilem lipidowym w surowicy badanych osób z terenu Bydgoszczy (Adv Clin Exp Med 2007,
16, 6, 743–749).
Słowa kluczowe: Chlamydophila pneumoniae, BMI, otyłość, nadwaga, cholesterol całkowity, triglicerydy, surowica.
According to reports from different areas, the
prevalence of overweight and obesity is increasing
at an alarming rate both in developed and develo−
ping countries. However, the estimated prevalence
rates of obesity vary worldwide [1–4]. The most
recent WHO data show that about 20% men and
30% women in European countries are obese [5].
According to a recent national survey in Poland,
over 50% of adults (19–59 years old) are overwe−
ight or obese [6]. The classical treatment of obesi−
ty based on increased physical activity and decre−
ased calorie intake has not been successful. The
lack of efficacy of this therapeutic approach is pro−
bably due to an incomplete understanding of the
precise etiology of obesity [7, 8]. The etiology of
obesity is multifactorial, as interactions between
nutritional, metabolic, cultural, behavioral, social,
and genetic factors are involved in the develop−
ment of obesity [1, 9–11]. There are also a number
of different lines of evidence indicating that vario−
us infections may be linked to obesity [12–16].
However, the possibility that viruses or bacteria
might be etiologic agents in human obesity has re−
ceived relatively little attention. One of these
agents is Chlamydophila pneumoniae, an intracel−
lular Gram−negative bacterium that commonly
causes acute as well as chronic respiratory infec−
tion [17]. It was suggested that C. pneumoniae in−
fection may be associated with an increase in bo−
dy mass index [15, 16]. There are also accumula−
ting data suggesting that C. pneumoniae infection
affects serum lipid concentrations [18–20].
The present study investigated the relationship
between overweight and lipid profile and evidence
of C. pneumoniae antibodies in a sample middle−
aged urban population from Bydgoszcz (Poland).
A relationship between C. pneumoniae infection
and asthma [21] and abdominal aortic aneurysm
[22] was observed in some Polish populations; ho−
wever, the present authors found no information
available on such an association with indices of
obesity in any social group in Poland and this stu−
dy was conducted to provide such pilot data.
Methods
Participants
The studied population consisted of 39 adult
subjects of whom four (10%) were male. The stu−
dy and control groups were recruited from the lo−
cal community (Bydgoszcz, Poland) by advertise−
ments in local pharmacies during the period from
March 2006 to April 2007. The subjects were in−
formed about the aim of this study and signed
a written consent form approved by local bioethics
committee. The participants were classified accor−
ding to their BMI (kg/m2) status as normal weight
(group A: control subjects) and overweight or obe−
se (group B: studied subjects). As recommended
by WHO, normal weight was defined as a BMI <
< 25 kg/m2, overweight as a BMI ≥ 25 kg/m2, and
obesity as a BMI ≥ 30 kg/m2 [1]. Anthropometric
measurements, which included height, weight, and
four skinfold thickness measurements (triceps, bi−
ceps, subscapular, and suprailiac), were used to
calculate the body mass index (BMI, kg/m2) and
the percentage of fat mass (%FM, %) [23]. Total
body fat was calculated using the Durnin and Wo−
mersley formula [24]. These anthropometric data
were obtained by, respectively, a height scale (Ra−
dwag, Poland), a digital electronic weighing scale
(Radwag), and an electronic skinfold caliper
(Skyndex I, USA).
Biochemical Analyses
Venous blood was drawn after overnight fa−
sting and the serum was separated from the red
cells by centrifugation at 3000 × g for 10 minutes.
The serum was immediately divided into aliquots
and frozen at –40°C until the serological assays
were performed. Total serum cholesterol (TChol,
mmol/l) and triglyceride (TG, mmol/l) levels were
determined by standard enzymatic methods with
reagents from Limarco, Poland. The analyses were performed on an automated BTS 310 analyzer
(Biosystems, Barcelona, Spain) in an accredited
analytical laboratory.
745
C. pneumoniae and Body Mass Index
Serological Analyses
The analyses of the IgG, IgA, and IgM Chla−
mydophila pneumoniae antibodies were perfor−
med using a commercially available enzyme−lin−
ked immunosorbent assay (ELISA, Vircell, Spain)
according to Gutierrez et al. [25]. First, 5 µl of pa−
tient serum, negative, positive, and cut−off con−
trols, and 100 µl of serum diluent were added to
each well (phosphate buffer). The microplate was
covered and incubated for 45 min at 37 C. After
incubation the strips was washed five times with
300 µl of washing solution (phosphate buffer). To
each well, 100 µl of conjugate (peroxidase labeled
anti-human IgG, IgM, or IgA antibodies) was added and the plate was incubated for 30 min at
37°C. The plate was washed as described above.
To each well, 100 µl of substrate solution (TMB,
tetramethylbenzidine) was added and the plate was
incubated at room temperature for 25 min. Finally,
50 µl of stop reagent (0.5 M H2SO4) was added to
each well and the optical density was measured.
Absorbance was read at 450 nm by an ELISA Microwell Plate Reader (Synergy HT, Bio-Tek Instruments Inc., USA). The results were determined
by calculating an index value from the optical density values relative to control materials [25]. The
index value was calculated by dividing the patient’s absorbance value by the mean absorbance
value of the cut-off point and then multiplied by
10. As recommended by the manufacturer, an
ELISA test index value > 11.0 was considered positive and < 9.0 negative [25].
Statistical Calculations
The results are given as the mean and standard
deviation or as a number (%). Differences between
the groups were tested by χ2 for categorical variables
and by the Mann Whitney U−test and Pearson’s cor−
relation for continuous variables. A p value ≤ 0.05
was considered statistically significant. The statisti−
cal analyses were carried out by STATISTICA PL
v. 6.1 software (Stat−Soft, Inc., Tulsa, OK, USA).
Results
The anthropometrical and biochemical charac−
teristics of the subjects and their serological status
are shown in Table 1. Of the 39 participants,
12 (30.8%) were of normal weight (group A) and
27 (69.2%) were overweight or obese (group B)
(Table 1). All the male subjects were classified in−
to group B. It was observed that the overwei−
ght/obese participants in group B had a higher fre−
quency of IgG and IgA seropositivity than the non−
obese subjects in group A. The prevalence of
serum IgG antibody for C. pneumoniae was 41.7%
in group A and 70.4% in group B and the presen−
ce of C. pneumoniae IgA antibodies was observed
in 16.7% of the non−obese group and in 40.7% of
Table 1. Characteristics of the studied populations
Tabela 1. Charakterystyka grupy badanej
Parameters
(Wskaźniki)
Non−obese, group A
(Z wagą należną, grupa A)
n = 12 (30.8%)
Overweight or obese, group B
(Otyli lub z nadwagą, grupa B)
n = 27 (69.2%)
p
Age – years)
(Wiek – lata)
37.7 ± 16.2
46.8 ± 11.9
0.125
BMI – kg/m2
22.7 ± 1.6
33.1 ± 4.5
0.000
%FM – %
31.9 ± 5.9
41.3 ± 5.3
0.000
TChol – mmol/l
5.19 ± 1.0
5.49 ± 0.87
0.298
TG – mmol/l
1.02 ± 0.3
1.41 ± 0.4
0.008
IgG positive – %
(IgG dodatni – %)
41.7
70.4
0.089
IgA positive (%)
(IgA dodatni – %)
16.7
40.7
0.140
IgG and IgA positive (%)
(IgG i IgA dodatni – %)
16.7
37.0
0.203
± SD – standard deviation.
p – statistical difference between groups A and B.
n – number of subjects (%).
± SD – odchylenie standardowe.
p – współczynnik istotności różnicy między grupami A i B.
n – liczność grupy (%).
746
A. JAWOROWSKA, G. BAZYLAK, E. GOSPODAREK
the overweight/obese. No subjects were positive
for IgM. Combined seropositivity for both IgG
and IgA antibodies suggestive of chronic infection
were present in 16.7% of the control group and
83.3% of the study group. Comparison of the non−
obese group and the overweight/obese group sho−
wed a significantly higher BMI, percentage of to−
tal body fat, waist/hip ratio, and serum triglyceride
level in the overweight/obese subjects. There were
no differences between the groups regarding age
and serum cholesterol (Table 1).
A significant relationship was observed be−
tween seropositivity for C. pneumoniae and selec−
ted variables in all subjects (Tables 2 and 3). In
those subjects who were seropositive for C. pneu−
moniae IgG antibodies, the mean BMI was signi−
ficantly higher than in the seronegative group
(31.4 ± 5.5 vs. 27.4 ± 6.3 kg/m2, p = 0.038). A si−
milar association was also observed for C. pneu−
moniae IgA antibody status, but this tendency was
not statistically significant. Subjects seropositive
for C. pneumoniae IgG and IgA antibodies had si−
gnificantly higher serum total cholesterol concen−
trations than seronegative subjects (5.64 ± 0.91 vs.
5.02 ± 0.81 mmol/l, p = 0.047, and 5.91 ± 0.67 vs.
5.15 ± 0.93 mmol/l, p = 0.007, respectively). Sero−
Table 2. Characteristics of the participants with positive and negative serology for
C. pneumoniae IgG antibody
Tabela 2. Wskaźniki antropometryczne i lipidowe a częstość wykrywania swoistych prze−
ciwciał anty−C. pneumoniae klasy IgG
Parameters
(Wskaźniki)
IgG Positive
(IgG+ seropozytywni)
n = 15 (38.46%)
IgG Negative
(IgG− seronegatywni)
n = 24 (61.53%)
p
Age – years
(Wiek – lata)
48.0 ± 12.6
39.5 ± 15.4
0.097
BMI – kg/m2
31.4 ± 5.5
27.4 ± 6.3
0.038
%FM – %
40.5 ± 5.2
35.2 ± 8.2
0.076
TChol – mmol/l
5.64 ± 0.91
5.02 ± 0.81
0.047
TG – mmol/l
1.38 ± 0.34
1.16 ± 0.49
0.047
± SD – standard deviation.
p – statistical difference between groups.
n – number of subjects (%).
± SD – odchylenie standardowe.
p – współczynnik istotności różnicy między grupami IgA− i IgA+.
n – liczność grupy (%).
Table 3. Characteristics of the participants with positive and negative serology for
C. pneumoniae IgA antibody
Tabela 3. Wskaźniki antropometryczne i lipidowe a częstość wykrywania swoistych prze−
ciwciał anty−C. pneumoniae klasy IgA
Parameters
(Wskaźniki)
IgG Positive
(IgG+ seropozytywni)
n = 13 (3.3%)
IgG Negative
(IgG− seronegatywni)
n = 26 (66.6%)
p
Age – years
(Wiek – lata)
52.2 ± 9.9
40.0 ± 13.9
0.008
BMI – kg/m2
31.6 ± 5.9
29.0 ± 6.2
0.208
%FM – %
40.7 ± 5.3
37.3 ± 7.5
0.168
TChol – mmol/l
5.91 ± 0.67
5.15 ± 0.93
0.007
TG – mmol/l
1.37 ± 0.32
1.26 ± 0.45
0.267
± SD – standard deviation.
p – statistical difference between groups.
n – number of subjects (%).
± SD – odchylenie standardowe.
p – współczynnik istotności różnicy między grupami IgA– i IgA+.
n – liczność grupy (%).
747
C. pneumoniae and Body Mass Index
positivity for C. pneumoniae IgG antibodies was
also associated with serum triglyceride concentra−
tion (TG), i.e. subjects with C. pneumoniae IgG
antibodies had significantly higher TG levels (1.38
± 0.34 vs. 1.16 ± 0.49 mmol/l, p = 0.047). There
were no differences in mean age between C. pneu−
moniae IgG antibody seropositive and seronegati−
ve subjects. However, seropositivity for C. pneu−
moniae IgA antibody was associated with age; in
this case, seropositive subjects were older than se−
ronegative (52.2 ± 9.9 vs. 40.0 ± 13.9, p = 0.008)
(Tables 2 and 3).
Positive correlations between C. pneumoniae
IgA antibody status and TChol (r = 0.42), and age
(r = 0.42) were observed. There were revealed al−
so positive associations between IgG antibody sta−
tus and TChol (r = 0.32), TG (r = 0.32), and BMI
(r = 0.34) (Table 4).
Discussion
The results of this study demonstrated that
subjects with positive serology for C. pneumoniae
IgG antibodies are characterized by higher BMI as
well as higher serum triglyceride and total chole−
sterol concentrations than those of the seronegati−
ve group, whereas seropositivity for C. pneumo−
niae IgA antibodies was associated with greater
age as well as higher total cholesterol concentra−
tion. The findings of this study are consistent with
the observations of Laurila et al. [18, 26] and Mur−
ray et al. [19] of raised serum total cholesterol and
triglyceride concentrations in randomly selected
samples of Finish and Irish adult male subjects, re−
spectively, with serological evidence of C. pneu−
moniae infection.
The data of the present study also show that the
prevalence of IgG and IgA antibodies and their
combined positive serology for C. pneumoniae is
about threefold higher in obese or overweight per−
sons than in non−obese individuals. There are two
possible explanations for the associations between
BMI and antibody status observed here. It is possi−
ble that infection with C. pneumoniae might be re−
lated to increased BMI. A second possibility is that
the degree of obesity might be a marker for greater
susceptibility to C. pneumoniae infection. Howe−
ver, it seems impossible that obese people would be
exposed to C. pneumoniae more often than normal
weight individuals. It was observed that overwei−
ght preadolescents were more susceptible to respi−
ratory infections [26]. However, there are also data
suggesting that increased BMI is associated with
impaired immunity [27–29]. Obesity is a predictor
of poorer antibody response to the hepatitis B vac−
cine [30, 31]. These findings induced Dhurandhar
et al. [12] to suggest that overweight or obese peo−
ple would be less likely to produce antibodies when
exposed to infection factors than normal−weight
people. Thus the prevalence of antibodies should
be similar or lower in obese than in lean people.
Evidence for an association of C. pneumoniae with
increased BMI in an urban population from Austra−
lia was also provided by Dart et al. [16], who obse−
rved significant differences in BMI between adult
subjects with coronary heart disease classified po−
sitive or negative for C. pneumoniae IgG antibo−
dies. It should also be noted that in the above study
[16], positive serology to other Chlamydia species
(C. psittaci and C. trachomatis) was extremely low
in the study group. Toplak et al. [15] revealed that
in a sample of elderly, non−diabetic subjects recru−
ited from Graz (Austria), the prevalence of seroac−
Table 4. Spearman’s Rank correlation coefficients between anthropometric,
lipid, and immunological status parameters
Tabela 4. Wartości współczynika Spearmana i współczynnika istotności cha−
rakteryzujące obserwowane korelacje między wskaźnikami antropometryczny−
mi, lipidowymi i immunologicznymi
Parameters
(Wskaźniki)
IgG status
IgA status
Spearman
r
p
Spearman
r
p
Age – year
(Wiek – lata)
0.27
0.096
0.42
0.008
BMI – kg/m2
0.34
0.035
0.21
0.204
%FM – %
0.29
0.072
0.23
0.164
TChol – mmol/l
0.32
0.046
0.42
0.007
TG – mmol/l
0.32
0.046
0.18
0.269
Significant correlations are marked in bold numbers.
Współczynniki korelacji istotnych statystycznie zaznaczono pogrubioną
czcionką.
748
A. JAWOROWSKA, G. BAZYLAK, E. GOSPODAREK
tive chlamydial infection was significantly higher
in the considerably overweight patients (BMI
> 30 kg/m2) compared with both moderately obese
and lean subjects. On the other hand, Ekesbo et al.
[32] found that combined seropositivity for
C. pneumoniae and Helicobacter pylori was highly
associated with obesity in a group of middle−aged
hypertensive patients living in an urban area in
Sweden. Quite recently, a similar relationship was
shown by Thjodleifsson et al. [33], who reported
a significant positive association between being
overweight (BMI > 25 kg/m2) and IgG antibody
status for C. pneumoniae and Helicobacter pylori
in a large multinational urban population study of
healthy middle−aged subjects from Iceland, Swe−
den, and Estonia. They suggested that infections
with C. pneumoniae and Helicobacter pylori are
both separately and synergistically associated with
overweight and this association is not related to in−
dicators of systemic inflammation such as C−reac−
tive protein (CRP) or serological markers related
with cagA protein and Toxoplasmosa gondii, hepa−
titis A virus (HAV), Esptein−Barr virus (EBV), her−
pes simplex virus 1 (HSV−1), and cytomegalovirus
(CMV) infection.
The authors conclude that the observations of
this study support the hypothesis that infections, in
this case C. pneumoniae infection, may be linked to
increased BMI. However, as this is hardly an obse−
rvational pilot study, these findings should still be
regarded only as suitable for generating working
hypotheses, mainly for women. The most serious
limitations of this study are the small sample size,
the disproportion in the sizes of the study and con−
trol groups, the female overrepresentation in both
these groups, and the lack of strictly age− and sex−
matched controls, so the authors are aware that the
presented results may not be amenable for genera−
lization. More detailed mechanisms by which
C. pneumoniae increases body weight are still unk−
nown, and the possibility cannot be excluded that
persons with overweight or obesity have an increa−
sed susceptibility to C. pneumoniae infection. Ho−
wever, these findings, despite the above−mentioned
shortcomings and limitations, are highly consistent
with the main conclusions of other studies perfor−
med previously in some European countries [15,
32, 33] and Australia [16] and should encourage
the design of a more advanced age− and sex−mat−
ched investigation to determine the range of health
status, sociodemographic, and socioeconomic fac−
tors modifying the possible association between
BMI and C. pneumoniae infection in urban and ru−
ral populations. To the authors’ best knowledge,
this pilot study is the first reported evidence of in−
fection−related obesity in Poland and the fourth
report in Europe, besides Austria [15], Sweden
[32, 33], Iceland [33], and Estonia [33].
Acknowledgements. The financial support of this study by the internal research grant CM−UMK−BW−68−2006 is
gratefully acknowledged.
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Address for correspondence:
Grzegorz Bazylak
Department of Bromatology and Molecular Nutrition
Faculty of Pharmacy
Collegium Medicum
Nicolaus Copernicus University
Jagiellońska 13
85−067 Bydgoszcz
Poland
Tel.: +48 52 585 39 15
E−mail: [email protected]
Conflict of interest: None declared
Received: 31.08.2007
Revised: 10.10.2007
Accepted: 6.12.2007