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European Journal of Heart Failure 2006 8(3):270-274; doi:10.1016/j.ejheart.2005.09.002
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© 2005 European Society of Cardiology

Relationship between cytokines and tumour markers in patients with chronic heart failure

Feridun Kosara,*, Yuksel Aksoya, Gulacan Ozguntekina, Ibrahim Ozerolb and Ercan Varolc

a Department of Cardiology, Inonu University, Faculty of Medicine, Turgut Ozal Medical Center 44069, Malatya, Turkey
b Department of Microbiology, Inonu University, Faculty of Medicine, Turgut Ozal Medical Center Malatya, Turkey
c Department of Cardiology, Isparta State Hospital Isparta, Turkey

* Corresponding author. Tel.: +90 223410660x4505; fax: +90 4223410728. E-mail addresses: mferidunkosar{at}yahoo.commferidunkosar{at}hotmail.com (F. Kosar).


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
Aims: Serum levels of some cytokines and tumour markers are elevated in patients with chronic heart failure (HF). We aimed to investigate the relationship between circulating levels of cytokines and tumour markers in patients with HF.

Methods: We included 35 HF patients and 33 normal controls. HF patients were divided into two groups: mild HF (NYHA class I/II) (n=10) and severe HF (NYHA class III/IV) (n=25). Serum cytokine levels (TNF-{alpha}, IL-1 ß, IL-6, and IL-10) were measured by ELISA and tumour markers (CA 125, CA 19-9, CA 15-3, CEA and AFP) by chemiluminescent enzyme immunoassay.

Results: Serum levels of TNF-{alpha}, IL-6, and IL-10 as cytokines, and CA 125 and CA 19-9 as tumour markers were significantly higher in HF patients than in normal controls (p<0.0001 for all). Serum levels of TNF-{alpha}, IL-6 and IL-10 and CA 125 in the severe HF patients were significantly higher than in the mild HF patients (p<0.001 for all). Correlation analysis showed that CA 125 was positively related to TNF-{alpha} (r=0.624, p<0.001), IL-6 (r=0.671, p<0.001), and IL-10 (r=0.545, p<0.001) in HF.

Conclusion: These findings show that CA 125 is markedly elevated in patients with HF, and correlates with serum TNF-{alpha}, IL-6 and IL-10 levels. Therefore, we speculate that among the tumour markers studied, only CA 125 is closely related to the cytokine system.

Key Words: Chronic heart failure • Cytokines • Tumour markers • CA 125

Received March 16, 2005; Revised June 7, 2005; Accepted September 6, 2005


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 References
 
Recent studies suggest that chronic heart failure may, in part, be an inflammatory disease. Cytokines, as inflammatory mediators, play a pivotal role in the pathogenesis of heart failure (HF) [1-5]. The determination of cytokine levels in serum facilitates monitoring of the immune and inflammatory responses to HF. Circulating pro-inflammatory cytokines such as tumour necrosis factor TNF-P and IL-6, and circulating anti-inflammatory cytokines such as IL-10 are increased in patients with chronic heart failure [6-10]. The development and progression of chronic heart failure can be explained by the known biological effects of these cytokines. For example, TNF-P and IL-6 produce negative inotropic effects on the heart [11,12]. Serum levels of these cytokines have also been shown to be related to clinical status, to hemodynamic abnormalities and to poor prognosis [13-15].

Measurement of tumour markers such as CA 125, CA 19-9, CA 15-3, AFP, and CEA, is currently used for screening, diagnosis, follow-up, prognostic stratification and therapeutic monitoring of different malignancies. Carbohydrate antigen 125 (CA 125) which is a high-molecular weight glycoprotein, is elevated particularly in patients with ovarian cancer [16-20]. Elevated serum CA 125 levels have also been reported in many other malignant and non-malignant diseases with pleural or pericardial fluids, regardless of the underlying etiology [17-28]. Recently, it has been reported that in patients with chronic heart failure, serum CA 125 levels are significantly elevated and that an increase in serum levels of CA 125 is correlated with the severity of disease [29-34]. Although increased levels of inflammatory cytokines and tumour markers such as CA 125 have been shown to be associated with heart failure, no report has yet shown that inflammatory cytokines themselves lead to elevated serum CA 125 levels.

The aim of the present study was to investigate the relationship between serum levels of pro-anti-inflammatory cytokines and tumour markers in patients with chronic heart failure.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 References
 
The present study included 35 consecutive heart failure patients (HF) (25 men and 10 women; aged 61.4±8.9 years) admitted to the Department of Cardiology, Inonu University Turgut Ozal Medical Center, Malatya, Turkey. Patients with stable heart failure were recruited from the outpatient clinics, decompensated patients were recruited from those admitted to our intensive care unit. On admission, the diagnosis of HF was based on medical history and initial investigation, which included physical examination, electrocardiogram, chest X-ray, and echocardiographic evaluation. The assessment of systolic cardiac function was performed by measuring left ventricular ejection fraction (LVEF) on echocardiography. All patients had a left ventricular ejection fraction of <40%. The aetiology of heart failure, determined by coronary angiography and cardiac catheterisation, was ischaemic heart disease in 14 patients and dilated cardiomyopathy in 21 patients. Clinical status of all patients was defined using the New York Heart Association (NYHA) classification. At the time of enrollment, patients were classified as either "mild" (NYHA class I or II) or "severe" (NYHA class III or IV) heart failure. Ten patients were classified as mild HF and 25 were classified as severe. Patients with renal failure, myocardial infarction within the previous 6 months, diabetes mellitus, infection or an inflammatory illness such as sepsis, malignancy, arthritis or connective tissue disease were excluded. At the time of the evaluation, patients were being treated with angiotensin-converting enzyme (ACE) inhibitors (56%), diuretics (62%), aldosterone antagonists (23%), digoxin (75%) and/or nitrates (18%). None were receiving antibiotics or anti-inflammatory drugs.

Thirty-three healthy age- and gender-matched volunteers served as a control group (24 men and 9 women; age 60.8±7.4 years). The healthy volunteers were all members of the hospital staff. None of the healthy volunteers had any concomitant disease, and all physical and laboratory examination parameters were normal. The control subjects did not undergo cardiac catheterization. The study protocol was approved by the hospital ethics committee, and all subjects gave informed consent prior to study entry.

2.1. Sample collection and blood tests
Blood was systematically taken from an antecubital vein at the time of or shortly after admission to the hospital. Blood samples were collected in tubes containing EDTA, immediately centrifuged and then stored at –80 C until assay.

2.2. Measurement of serum cytokines and serum tumour markers
Serum cytokine levels (TNF-P, IL-1β, IL-6, and IL-10) were measured using commercially available Enzyme Linked Immuno-Sorbent Assay (ELISA) kits (BioSource International, Inc, California, U.S.A.), serum levels of the tumour markers [CA 125, CA 19-9, CA 15-3, carcinoembryonic antigen (CEA), and alpha-fetoprotein (AFP)] were determined simultaneously by chemiluminescent enzyme immunoassay methods, using OM-MA, BR-MA, GI-MA, CEA and AFP commercial kits in sequence, respectively (DPC, Los Angeles, USA).

2.3. Echocardiographic assessment
All patients underwent a two-dimensional Doppler echocardiographic examination (ATL system HDI 5000 ultrasound) within 2 h of admission. Echocardiographic examination included measurement of left ventricular end-diastolic (LVEDD) and end-systolic diameters (LVESD), estimation of left ventricular ejection fraction (LVEF) using the Simpson method and checking for the presence of pericardial fluid. Systolic pulmonary artery pressure was estimated non-invasively by peak flow velocity of tricuspid regurgitation on continuous wave Doppler using a Standard approach.

2.4. Statistical analysis
Continuous variables are presented as mean±SD. The differences between the study groups were evaluated using unpaired t test and Kruskal-Wallis H tests as appropriate. Pearson's correlation test was used to analyze the relationship between cytokines and tumour markers. A p value<0.05 was considered as statistically significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 References
 
The heart failure patients did not differ from the normal controls with regard to age, sex and body mass index. Serum levels of TNF-P, IL-6 and IL-10 in the patient group were significantly higher than in the control group (7.65±2.3 vs. 1.32±0.76 pg/ml; p<0.001, 15.3±2.6 vs. 4.3±1.2 pg/ml; p<0.001, 17.9±3.2 vs. 9.2±2.5 pg/ml; p<0.001, respectively). There was no difference in IL-1β levels between the study groups. Statistically significant differences were found for TNF-P, IL-6 and IL-10 between NYHA Class I/II and III/IV groups (4.97±1.27 vs. 8.72±1.65 pg/ml; p<0.001, 12.7±2.2 vs. 16.4±3.1 pg/ml; p<0.001, 13.8±3.4 vs. 19.6±2.8 pg/ml; p<0.001, respectively) (Table 1). However, there was no difference in serum IL-1β levels between the mild and severe heart failure groups.


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  		Table 1 Comparison of serum inflammatory cytokine and tumour marker levels in normal controls and in heart failure patients according to NYHA class

 
Serum CA 125 and CA 19-9 levels were significantly higher in the HF patient group than in the normal control group (59.8±9.5 vs. 7.2±3.0 U/ml; p<0.001, 16.6±1.9 vs. 6.2±1.2 U/ml; p<0.001). However, no statistically significant difference was found between the patient and control groups for the other tumour markers. Serum CA 125 levels in the NYHA Class III/IV group were significantly higher than in the NYHA Class I/II group (39.2±4.0 vs. 68.1±12 U/ml; p<0.001) (Table 1). There were no statistically significant differences for any other tumour markers between the functional class groups.

Correlation analysis showed that serum CA 125 levels were significantly associated with TNF-P (r=0.624, p<0.001) (Fig. 1), IL-6 (r=0.671, p<0.001) (Fig. 2), and IL-10 (r=0.545, p<0.001) (Fig. 3) in the HF patients. However, there were no other significant correlations between tumour markers and cytokines.


Figure 1
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  		Fig. 1 Positive linear correlation between serum TNF-P and CA 125 levels.

 


Figure 2
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  		Fig. 2 Positive linear correlation between serum IL-6 and CA 125 levels.

 


Figure 3
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  		Fig. 3 Positive linear correlation between serum IL-10 and CA 125 levels.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
References
 
The relationship between serum cytokines and tumour markers in heart failure is an area of increasing interest. It is known that certain cytokines play an important role in the pathogenesis of chronic heart failure and its prognosis [1-6]. Also, it has been reported that HF patients have increased serum CA 125 levels [29-34]. Until now, there was no data available on the relationship between pro- and anti-inflammatory cytokines and tumour markers in patients with chronic heart failure. To our knowledge, this is the first study to investigate the potential relationship between these cytokines and tumour markers in heart failure patients.

The present study shows that heart failure patients have markedly elevated serum levels of TNF-P, IL-6, and IL-10 as compared to normal controls, and that this increase parallels the severity of HF. Serum IL-1β levels were not different between the patients and the controls and also did not change with the severity of HF. These findings are consistent with the findings of other investigators [6-15]. Since serum cytokines may be elevated due to acute or chronic infections and inflammation, we excluded these conditions in the present study. In addition, in order to minimize the effect of medication, patients receiving antibiotic or anti-inflammatory agents were not included in the study. In the evaluation of tumour markers, we only observed high serum levels of CA 125 and CA 19-9 in the HF patients compared with the normal controls, the increase in serum CA 125 levels was significant in patients with severe HF (NYHA III-IV), compared to those with mild HF (NYHA class I-II). In other words, serum CA 125 levels increased in parallel with the severity of heart failure which is consistent with the findings of previous studies [29-34]. Although serum CA 19-9 levels had a tendency to increase with the severity of the disease, this difference was not significant.

Elevated CA 125 levels have been reported in ovarian cancer, lymphoma, gastrointestinal tract, lung and uterine malignancies [16-25]. Previous studies have shown that high levels of serum CA 125 are associated with the presence of benign and malignant serosal fluids [26-28]. Turk et al. [29] found that serum CA 125 levels were significantly higher in heart failure patients with pleural effusion than in those without pleural effusion. A recent study performed by Varol et al. [31] reported that serum CA 125 levels may be related to the presence and severity of heart failure and also the presence of pericardial effusion. These reports suggest that serosal fluids occurring in patients with HF appear to be directly responsible for elevated serum CA 125 levels, and that the presence of serosal fluid may stimulate its release rather than its cytopathological content. In other words, it is suggested that the increase in serum CA 125 levels may be due to production by mesothelial cells and non-mesothelial cells as a consequence of inflammation, stasis or other stimulatory mechanisms. Duman et al. [32] suggested that in HF patients with mitral stenosis, elevated CA 125 levels may be due to venous congestion and activation of peritoneal mesothelial cells or increased signal peptides.

Recently, Nagele et al.[33] investigated serum CA 125 levels in heart failure patients undergoing evaluation for cardiac transplantation. They showed that there was an increase in serum CA 125 levels in both advanced heart failure patients in whom fluid accumulation may be possible and in mild heart failure patients in whom serosal effusion is not expected. D'Aloia et al. [34] showed elevated serum CA 125 levels both in the few patients with pleural, pericardial or peritoneal effusion and in most patients with moderate to severe heart failure with no effusion. Our study showed that, in addition to the elevation in advanced heart failure patients, serum CA 125 levels were significantly increased in the mild heart failure patients with no serosal effusion. In other words, these findings in mild heart failure patients indicate that elevated serum CA 125 levels may be dependent not only on serosal stimulation, but also on inflammation as a consequence of cytokine network activation. Our most striking finding was that the increase in serum CA 125 levels was positively correlated with serum TNF-P, IL-6, and IL-10 levels, suggesting that serum CA 125 levels have a strong positive relationship with serum TNF-P, IL-6, and IL-10 levels in HF patients. In this sense, our study supports the hypothesis that elevated serum CA 125 levels are closely associated with inflammatory mediators or cytokines. Accordingly, previous reports have suggested that CA 125 is produced and secreted from ovarian epithelial tumour cells and lymphoma, when stimulated by cytokines such as TNF-P and IL-6 [35,36]. As a result of this, we speculate that in heart failure, inflammatory cytokines such as TNF-P, IL-6, and IL-10 may either permit expression of CA 125 or predispose to contributory factors for the production of CA 125.

4.1. Conclusion
Our study shows that serum CA 125 levels are elevated in patients with HF and also that this increase in serum CA 125 levels correlates with TNF, IL-6 and IL-10 but not with IL-1 β. These data suggest that a link may exist between the cytokines and CA 125 in HF patients. In other words, elevated serum CA 125 levels may be secondary to the activation of these cytokines in these patients. Further studies are required to validate our data. The findings of this study are limited by the small patient numbers and the selected population.


   Acknowledgements
 
We thank to Saim Yologlu for the help in the evaluation of statistical analysis.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 

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