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ORIGINAL ARTICLE
Year : 2019  |  Volume : 32  |  Issue : 1  |  Page : 212-216

Estimation of serum testosterone and luteinizing hormone levels in male patients with chronic obstructive pulmonary disease


1 Department of Chest, Menoufia University, Shebin Elkom, Egypt
2 Department of Medical Biochemistry, Menoufia University, Shebin Elkom, Egypt
3 Department of Pulmonology, ministry of Health, El-Mahalla Chest Hospital, Gharbeya, Egypt

Date of Submission21-May-2017
Date of Acceptance24-Jul-2017
Date of Web Publication17-Apr-2019

Correspondence Address:
Ibrahim A Albana
Qtour Gharbeya
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_372_17

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  Abstract 


Objective
The aim of this study was to assess serum testosterone in patients with chronic obstructive pulmonary disease (COPD) and discuss the impacts of decreased serum testosterone levels as an anabolic hormone.
Background
Decreased levels of anabolic hormone may occur in COPD patients; thus, both serum testosterone and luteinizing hormone levels should be investigated.
Participants and methods
This case–control study was carried out in El-Mahalla Chest Hospital from October 2015 to February 2016. A total of 55 individuals were enrolled in the study: 35 adult male COPD patients and 20 age-matched men as a control group. All participants were subjected to a detailed assessment of history, clinical examination, chest radiography, O2saturation, spirometry [measurement of forced expiratory volume in 1 s (FEV1)/forced vital capacity (FVC), FVC, FEV1% of predicted], complete blood picture, liver function tests, kidney function tests, and random blood sugar; also, both serum testosterone and luteinizing hormone levels were measured using direct chemiluminescent technology.
Results
The smoking index of the COPD patients was 66.06 ± 6.83 pack-years and that of the control group was 11.25 ± 1.86 pack-years, with a highly statistically significant difference between both groups (P < 0.001). Oxygen saturation of COPD patients was 92.51 ± 1.77% and that of the control group was 96.45 ± 0.69%, with a highly statistically significant difference between the two groups (P < 0.001). In terms of the FEV1/FVC ratio, FEV1% and FVC% were highly statistically significantly lower in COPD patients compared with the control participants (P > 0.001). Testosterone was highly statistically significantly lower in COPD patients compared with the control group (P > 0.001).
Conclusion
Disturbances in serum testosterone hormone levels in COPD patients were correlated with smoking, FEV1, and hypoxemia.

Keywords: chronic obstructive pulmonary disease, hypogonadism, luteinizing hormone, testosterone


How to cite this article:
Mansour OF, El Wahsh RA, El Hefnawy MY, Abd El Gayed EM, Albana IA. Estimation of serum testosterone and luteinizing hormone levels in male patients with chronic obstructive pulmonary disease. Menoufia Med J 2019;32:212-6

How to cite this URL:
Mansour OF, El Wahsh RA, El Hefnawy MY, Abd El Gayed EM, Albana IA. Estimation of serum testosterone and luteinizing hormone levels in male patients with chronic obstructive pulmonary disease. Menoufia Med J [serial online] 2019 [cited 2019 May 27];32:212-6. Available from: http://www.mmj.eg.net/text.asp?2019/32/1/212/256107




  Introduction Top


Chronic obstructive pulmonary disease (COPD) is a growing cause of morbidity and mortality worldwide and will be the third leading cause of death by 2030 [1].

Systemic inflammation and physical inactivity have been identified as relevant extra pulmonary markers of the severity of COPD as both conditions are related to exacerbations, hospitalizations, and mortality in these patients [2].

The respiratory system is not the only system considered to be affected by COPD; also the rest of the body can also be affected. The systemic manifestations of COPD involve a number of endocrine disorders such as those involving the pituitary, the thyroid, the gonads, the adrenals, and the pancreas [3].

Several functions such as mood, sexual desire, formation of bone, metabolism, erythropoiesis, estrogen precursor, and primary and secondary male sex characteristics depend on the testosterone hormone [4].

Patients with COPD have a chronic illness. They are commonly hypoxemic, hypercapnic, or both, have increased levels of systemic inflammatory markers, and receive glucocorticoids. Each of these factors can affect endocrine function. In turn, altered endocrine function can worsen COPD [3].

Spermatogenesis regulation requires the luteinizing hormone (LH), which stimulates the synthesis of testosterone, which plays a main role in spermatid maturation [5].

Under physiological conditions, about 44% of circulating testosterone is strongly bound to the sex hormone-binding globulin; 4% is weakly bound to albumin and other lower affinity, high-capacity binding sites, such as acid glycoprotein and transcortin. About 2% of circulating testosterone is nonprotein bound, i.e. free testosterone. Together, weakly bound testosterone and free testosterone are referred to as 'bioavailable testosterone' [6].

Several conditions such as cachexia, osteoporosis, sexual dysfunction, and immunological and memorial disturbances in response to decreased anabolic hormones have been described in COPD and other diseases [7].

Therefore, the aim of this study is to assess serum testosterone in patients with COPD and discuss the impacts of decreased serum testosterone levels as an anabolic hormone.


  Participants and Methods Top


This case–control study was carried out in El-Mahalla Chest Hospital. All patients admitted to the hospital from October 2015 to February 2016 were included in the study and a total of 35 patients were studied. Twenty age-matched men were included as a control group. After obtaining the approval of the ethics committee of the Menoufia Hospital's Review Board and a written informed consent from all participants, each one of them were subjected to the following. Assessment of medical history: clinical (general and chest) examination and O2 saturation by pulse oximetry (SO2).

Radiological examination: plain chest radiography

Laboratory investigations: complete blood picture, liver function tests, kidney function tests, and random blood sugar.

Measurement of serum levels of the gonadal hormones (testosterone and LH): a sample of venous blood sample was obtained from the participants in the morning, centrifuged, and the serum was stored at −80°C until analysis by direct chemiluminescent technology.

Spirometry with reversibility testing: spirometry was performed in the pulmonary function test unit in Mahala Chest Hospital using Chestgraph HI-105 apparatus (Hongo Bunkyo-ku, Tokyo, Japan). Slow and forced vital capacities [forced vital capacity (FVC%) of predicted], prebronchodilator and postbronchodilator forced expiratory volume in 1 s (FEV1% of predicted), and FEV1/FVC were all measured, and all participants were classified according to the Global Initiative for Chronic Obstructive Lung Disease classification [8].

Statistical analysis

Data were analyzed using SPSS software package version 20.0 (IBM Corp, Armonk, New York, USA). The Kolmogorov–Smirnov test was used to verify the normality of distribution of variables; Student's t-test was used to compare two groups for normally distributed quantitative variables. The Mann–Whitney test was used to compare two groups for abnormally distributed quantitative variables. Spearman's coefficient was used to correlate between quantitative variables. All tests were used as tests of significance at a P value less than 0.05 level.


  Results Top


Patients and controls were comparable in terms of age and BMI (P > 0.05); the mean age of the COPD patients was 54.69 ± 8.27 years and that of the control group was 52.65 ± 4.56 years. BMI of the COPD patients was 23.29 ± 3.12 kg/m 2, whereas that of the controls was 23.73 ± 2.43 kg/m 2 [Figure 1] and [Figure 2].
Figure 1: Correlation between serum testosterone and the smoking index in COPD patients. COPD, chronic obstructive pulmonary disease.

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Figure 2: Correlation between serum testosterone and FEV1 in COPD patients. COPD, chronic obstructive pulmonary disease; FEV1, forced expiratory volume in 1 s.

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The smoking index of the COPD patients was 66.06 ± 6.83 pack-years and that of the control group was 11.25 ± 1.86 pack-years, with a highly statistically significant difference between both groups (P < 0.001). Oxygen saturation of the COPD patients was 92.51 ± 1.77% and that of the control group was 96.45 ± 0.69%, with a highly statistically significant difference between the groups (P < 0.001). For the FEV1/FVC ratio, FEV1% and FVC% were highly statistically significantly lower in COPD patients compared with the control participants (P > 0.001) [Table 1].
Table 1: Comparison between the studied groups in FEV1/FVC, FEV1%, FVC% predicted, smoking index, and SaO2%

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Testosterone was highly statistically significantly lower in COPD patients compared with the control group (P > 0.001). There was no statistically significant difference between the patient group and the control group in LH levels in serum (P = 0.523) [Table 2].
Table 2: Comparison between the studied groups in testosterone and luteinizing hormone

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Serum testosterone level was correlated positively with FEV1% and correlated negatively with the smoking index [Table 3].
Table 3: Spearman's correlation between testosterone and LH with different parameters in all participants

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  Discussion Top


COPD is a common preventable and treatable disease characterized by persistent airflow limitation that is usually progressive and associated with an enhanced chronic inflammatory response in the airways and the lung to noxious particles or gases. Exacerbations and comorbidities contribute toward the overall severity in individual patients [8].

Comorbidities such as chronic heart failure, cardiovascular disease, depression, diabetes, muscle wasting, weight loss, lung cancer, and osteoporosis can be found frequently in patients with COPD and are considered to be part of the commonly prevalent non pulmonary sequelae of the disease [9].

In the present study, serum testosterone level was 4.72 ± 2.42 ng/ml in COPD cases and 6.73 ± 0.91 ng/ml in the control participants, with a highly statistically difference between the two groups.

These results were in agreement with those of Karadag et al. [7], who reported that testosterone levels were lower in COPD patients compared with control participants.

In this study, the serum LH level was 8.89 ± 3.57 mIU/ml in COPD cases and 7.88 ± 1.51 mIU/ml in the control group, with no statistically difference between the two groups.

However, Creutzberg et al. [10], who assessed the relation between sex hormone status and the stage of COPD, concluded that the intensity of sex hormone changes was correlated with the stage of COPD. As the severity of disease increased, testosterone decreased and both LH and follicle-stimulating hormone increased compensatively.

This study shows that the correlation between serum testosterone level and the smoking index was significantly negative in the COPD group.

In contrast, English et al. [11] reported no relation between serum testosterone level and smoking.

Although oxygen saturation showed a highly statistically significant difference between both groups, no correlation was found between serum testosterone level and oxygen saturation in COPD patients.

In contrast, Karadag et al. [7] reported decreased serum testosterone level in patients with COPD and the decline in testosterone level was correlated to the severity of the decline in FEV1, hypoxemia, and hypercapnia.

In this study, a positive significant correlation was found between serum testosterone level and FEV1 in COPD patients.

This significant correlation between the testosterone levels and the severity of airway obstruction further supports the fact that the high prevalence of hypogonadism in COPD patients is related to the pathogenesis of the disease and is different from the late-onset hypogonadism that occurs in the general population. Chronic illnesses such as diabetes mellitus, cardiovascular disease, and hypertension have been associated with a decline in serum testosterone. COPD is a chronic illness and hence may result in testosterone deficiency. Our results are similar to those of Karadag et al. [7], who studied a group of patients with stable COPD and patients in an exacerbation, and found that testosterone and dehydroepiandrosterone sulfate levels were lower in patients with severe COPD (FEV1 <50%) and detected a positive correlation between testosterone and FEV1. Makarevich et al. [12] assessed the relation between sex hormone status and the stage of COPD. They concluded that the intensity of sex hormone changes was correlated with the stage of COPD. As the severity of disease increased, testosterone decreased, whereas LH and follicle-stimulating hormone increased in compensation. Also, Shaker et al. [13] studied the sex hormone levels in COPD patients during exacerbation and after 1 m found that the low levels of serum testosterone found in these patients were significantly correlated to the severity of airway obstruction as measured by FEV1%.

This result was in agreement with Mousavi et al. [14], who found that FEV1 was correlated with the level of serum testosterone.

Also, Kaparianos et al. [15] reported that the levels of testosterone were correlated to FEV1, hypoxemia, and systemic inflammation among mild, moderate, and severe COPD groups of patients.

Leydig cells in gonads responsible for the secretion and synthesis of testosterone and hypophysis secreted LH to control testosterone secretion [4].

The increase in LH represents a compensatory action of the axis between gonads' pituitary and the hypothalmus to correct the decrease in testosterone levels in COPD patients [16].

Although our study showed no relations between LH and all parameters, several studies such as those of Laghi et al. [17] and Abd El Dayem et al. [18] reported increased LH as a compensatory mechanism for decreased testosterone levels.

Some studies have indicated that low circulating levels of testosterone are common in men with COPD; one trial reported a 30% incidence of hypogonadism among these patients. Still little is known about the actual prevalence, underlying causes, and the functional consequences of hypogonadism in patients with COPD. Most patients with COPD are middle-aged or older, and by definition, all have a chronic illness. It is estimated that 20% of men from 60 to 80 years of age have serum testosterone levels below the lower limit of normal; thus, aging and chronic illness have been associated with a decline in serum testosterone, the so-called androgen deficiency [10],[19],[20].


  Conclusion Top


Late-onset hypogonadism was found in patients with COPD compared with the controls. Alterations in sex hormone levels of male COPD patients are related to smoking, decline of FEV1, and hypoxia. Late-onset hypogonadism could develop in COPD patients as part of multiple comorbidities and systemic consequences; thus, future researches in this area are needed to shed more light on the prevalence and effects of COPD comorbidities. More researches are also required especially on the role of testosterone replacement therapy in the prevention of hypogonadism and in COPD patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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World Health Organization. Evidence-informed policy-making 2016. Available from: http://www.who.int/evidence. [Last accessed on 2017 Feb 10].  Back to cited text no. 1
    
2.
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Griffin JE. Male reproductive function. In: Griffin JE, Ojeda SR. Textbook of endocrine physiology. 5th ed. New York, NY: Oxford University Press; 2004. 226–248.  Back to cited text no. 6
    
7.
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8.
Global Initiative for Chronic Obstructive Lung Disease (GOLD). Global strategy for the diagnosis, management and prevention of chronic obstructive pulmonary disease, 2017. Available from: http://www.goldcopd.org. [Last accessed on 2017 Apr 12].  Back to cited text no. 8
    
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Magnussen H, Watz H. Systemic inflammation in COPD and asthma. Proc Am Thorac Soc 2009; 6:648–651.  Back to cited text no. 9
    
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Creutzberg EC, Casaburi R. Endocrinological disturbances in chronic obstructive pulmonary disease. Eur Respir J 2003; 22 (Suppl 46):76s–80s.  Back to cited text no. 10
    
11.
English KM, Pugh PJ, Parry H, Scutt NE, Channer KS, Jones TH. Effect of cigarette smoking on levels of bioavailable testosterone in healthy men. Clin Sci (Lond) 2001; 100:661–665.  Back to cited text no. 11
    
12.
Makarevich AE. Disorders of sex hormone status in patients with chronic obstructive pulmonary disease. Wiad Lek 2003; 56:140–146.  Back to cited text no. 12
    
13.
Shaker A, El-Shora A, El-Gammal M, Labib HA. Endocrinal disturbances and systemic inflammatiom in chronic obstructive pulmonary disease (COPD). Egypt J Chest Dis Tuber 2012; 61:81–88.  Back to cited text no. 13
    
14.
Mousavi SA, Kouchari MR, Samdani SH, Gilvaee ZN, Arabi M. Relationship between serum levels of testosterone and the severity of chronic obstructive pulmonary disease. Tanaffos 2012; 11:32–35.  Back to cited text no. 14
    
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Kaparianos A, Argyropoulou E, Efremidis G, Spiropoulos K. Sex hormone alterations and systemic inflammation in a group of male COPD smokers and their correlation with the + 138 insA/delA endothelin-1 gene polymorphism. A case–control study. Eur Rev Med Pharmacol Sci 2011; 15:1149–1157.  Back to cited text no. 15
    
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Morley JE, Kaiser FE, Perry HM, Patrick P, Morley PM, Stauber PM. Longitudinal changes in testosterone, luteinizing hormone, and follicle-stimulating hormone in healthy older men. Metabolism 1997; 46:410–413.  Back to cited text no. 16
    
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Laghi F, Langbein WE, Antonescu TA, Jubran A, Bammert C, Tobin MJ. Respiratory and skeletal muscles in hypogonadal men with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2005; 171:598–605.  Back to cited text no. 17
    
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    Figures

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  [Table 1], [Table 2], [Table 3]



 

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