Introduction

Several areas of the world, Latin America in particular, have undergone deep a socioeconomic and demographic transformation accompanied by changes in the lifestyle, dietary habits, and patterns of disease prevalence. As a consequence, the numbers of obese individuals and patients with metabolic syndrome (MS) have exhibited remarkable increases in Latin America [1]. Recent data from the Brazilian Health Ministry show that obesity and overweight rate are increasing in prevalence. According to the World Health Organization (WHO) criteria, the proportion of individuals with overweight in Brazil (BMI between 25 and 29.9 kg/m2) increased from 42.7 % in 2006 to 48.5 % in 2011, while the percentage of obese people (BMI ≥30 kg/m2) increased from 11.4 to 15.8 % in the same period [2, 3]. The treatment of obesity is usually complex and requires a multidisciplinary approach, ranging from behavioural changes to bariatric surgery. The intragastric balloon (IGB) is one such option, considered a low risk procedure and with satisfactory results in the short term [4]. A recent meta-analysis reported average weight loss of 12.2 % and body mass index (BMI) reduction of 5.7 kg/m2 when IGB was used over a 6-month period [4].

Obesity causes alterations of lung function. Several factors interfere with the respiratory mechanics in obese individuals. Excess adipose tissue induces mechanical compression on the diaphragm, lungs, and chest, which might lead to restrictive respiratory failure [5]. As a function of the inefficacy of the respiratory muscles, their strength and endurance might be reduced in obese [6]. Interestingly, because MS also alters lung function, the lungs might be exposed to greater damage in MS combined with obesity than in either condition alone [7].

Dual-energy X-ray absorptiometry (DXA) has been increasingly used to assess obesity [8]. DXA has revealed a correlation between the lung function and body fat distribution of obese patients [9]. Studies that used DXA suggest that fat deposition in the trunk and a predominance of the gynoid pattern of distribution bear a close correlation with the decline of lung function [10]. Other studies showed that, in men, the lean mass exerts a positive influence on lung function, whereas the influence of central fat deposition is negative [11].

Studies that assessed weight loss induced by either bariatric surgery or low-calorie diets showed that lung function improves as BMI decreases [12]. However, there are no data on the use of IGB and the effects of the associated weight loss on lung function, the pattern of body fat deposition, and the parameters of MS. Therefore, the primary aim of our study was to perform a longitudinal analysis of the effects of IGB on lung function, DXA parameters, and MS indicators. In addition, we assessed the correlation between changes in lung function and the effects of weight loss on the MS and DXA parameters after 6 months of use of IGB.

Patients

This was a longitudinal and interventional study conducted from June 2011 to September 2012 with 52 patients aged 18 to 65 years. All the participants exhibited overweight or obesity according to the WHO criteria [2] in addition to MS according to the criteria of the International Diabetes Federation [13]. The exclusion criteria were type 1 or 2 diabetes mellitus, pregnancy, previous stomach surgery, hiatal hernia ≥5 cm, clotting disorders, potentially bleeding gastrointestinal lesions, and alcoholism or use of drugs. The study was approved by the institutional research ethics committee. All patients signed an informed consent form. The study is registered at ClinicalTrials.gov (identifier, NCT01598233).

Methods

MS was defined by the presence of central obesity (waist circumference (WC) >80 cm in women and >90 cm in men), arterial hypertension (arterial pressure ≥130/85 mmHg), increased blood glucose (fasting glycaemia ≥100 mg/dL or diagnosis of diabetes mellitus), hypertriglyceridaemia (triglycerides ≥150 mg/dL or treatment for dyslipidaemia), and reduced high-density lipoprotein (HDL) (<40 mg/dL in men or <50 mg/dL in women) [13].

A silicone IGB (Silimed Silicone Instrumental Médico-cirúrgico Hospitalar Ltda, Rio de Janeiro, RJ, Brazil) was implanted by upper gastrointestinal endoscopy under deep sedation. Under endoscopic visualisation, the IGB was placed in the stomach and filled with 650 mL of normal saline solution (0.9 % NaCl) and 20 mL of methylene blue solution. According to local regulations and our institutional ethics committee, all patients remained in the hospital up to 24 h following the procedure [14].

The lung function parameters were assessed before IGB implantation and after IGB removal by spirometry, static pulmonary volumes using the helium dilution, carbon monoxide lung diffusion capacity (DLco), muscle inspiratory strength (MIP), and muscle expiratory strength (MEP). The tests were performed using Collins Plus Pulmonary Function Testing Systems (Warren E. Collins, Inc., Braintree, MA, USA). Brazilian reference values were used [15–18].

The pattern of body fat distribution was assessed by DXA using a Prodigy-GE densitometer (GE Healthcare, Inc., Madison, WI, USA). The tests were performed before implantation and immediately after the removal of the IGB. The truncal pattern of fat distribution was characterised by preferential fat deposition in the trunk, the android pattern by fat deposition in the abdomen, and the gynoid type by fat deposition in the gluteal–femoral area [19].

Statistical Analysis

The data are expressed as median and interquartile range or as frequencies. Non-parametric methods were used because most of the variables related to lung function did not exhibit a normal distribution according to the Shapiro–Wilk test. The changes in pulmonary function, MS, and DXA after 6 months of IBG use were assessed by the Wilcoxon signed-rank test or McNemar’s test. The participants were divided in two subgroups based on the presence or absence of MS after the removal of IGB, and the absolute changes in the lung function variables between these two subgroups were assessed by the Mann–Whitney test. The correlations were analysed by Spearman’s correlation coefficient. The level of significance was established as 5 %. Statistical analysis was performed using SAS v.6.11 (SAS Institute, Inc., Cary, NC, USA).

Results

The initial sample comprised 52 patients, six of whom were excluded because they exhibited complications that required early IGB removal: five because of gastric intolerance and one due to rupture of the device. All these complications occurred within the first 8 weeks of IGB use. Another six patients did not perform the lung function tests on schedule and were also excluded. Therefore, 40 patients completed the study. DXA before and after treatment was performed in 31 participants because the tests could not be performed in six patients due to technical reasons (excess weight) and three participants missed the appointments.

At the initial assessment of BMI, two participants (5 %) were overweight, five (12.5 %) had grade 1 obesity, 16 (40 %) had grade 2 obesity, and 17 (42.5 %) had grade 3 obesity. Twelve (30 %) participants exhibited restrictive ventilatory disorder, and in one (2.5 %) the FEV1/FVC ratio was lower than 0.70. The initial values of lung function parameters are listed in Table 1.

Table 1 Values of pulmonary function at baseline
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After 6 months of IGB use, only five (12.5 %) participants exhibited restrictive ventilatory disorder, none a FEV1/FVC ratio lower than 0.70, the MIP was reduced in 22 (55 %), and the MEP in 35 (87.5 %). DLco was reduced in three participants (7.5 %) and elevated in three others. Table 2 lists the effects of the use of IGB on weight, body mass index, and lung function parameters during the study. The weight lost at IGB removal was 11.8 % (7.3–20.2 %) of the initial weight.

Table 2 Effects of intragastric balloon on weight, body mass index, and lung function parameters over a 6-month period
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At the end of the study, only nine participants (22.5 %) met the diagnostic criteria of MS. Additionally, the parameters of body fat distribution assessed by DXA exhibited remarkable changes. These data are shown in Table 3.

Table 3 Effects of intragastric balloon on metabolic syndrome and dual energy X-ray absorptiometry parameters over a 6-month period
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Table 4 and Figs. 1, 2, and 3 show the correlations between the changes in lung function parameters and the changes in MS variables during the study. Table 5 and Figs. 4 and 5 list the correlations between the changes in lung function variables and the changes in DXA variables in the same 6-month period. A comparison of the participants with MS improvement to the ones without improvement did not find significant differences in the changes in lung function variables between these groups (p < 0.05).

Table 4 Spearman’s correlation coefficients between the changes in the variables of lung function and metabolic syndrome
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Fig. 1
figure 1

Relationship of absolute variation of total lung capacity (TLC) with absolute variation of waist circumference over a 6-month period (ρ = −0.34; p = 0.03); correlation was determined using Spearman’s rank correlation

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Fig. 2
figure 2

Relationship of absolute variation of functional residual capacity (FRC) with absolute variation of body mass index (BMI) over a 6-month period (ρ = −0.39; p = 0.01); correlation was determined using Spearman’s rank correlation

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Fig. 3
figure 3

Relationship of absolute variation of expiratory reserve volume (ERV) with absolute variation of body mass index (BMI) over a 6-month period (ρ = −0.44; p = 0.005); correlation was determined using Spearman’s rank correlation

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Table 5 Spearman’s correlation coefficients between the changes in the variables of lung function and dual energy X-ray absorptiometry
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Fig. 4
figure 4

Relationship of absolute variation of expiratory reserve volume (ERV) with absolute variation of trunk fat mass over a 6-month period (ρ = −0.51; p = 0.004); correlation was determined using Spearman’s rank correlation

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Fig. 5
figure 5

Relationship of absolute variation of expiratory reserve volume (ERV) with absolute variation of whole-body fat mass over a 6-month period (ρ = −0.59; p = 0.0005); correlation was determined using Spearman’s rank correlation

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Discussion

The main finding of the present study was a significant BMI reduction following 6 months of IGB use. In addition, there was a statistically significant improvement for both the MS parameters and pulmonary function variables. A significant fat percentage reduction was observed in all assessed body areas. To the best of our knowledge, this is the first study that has found a positive effect with the use of IGB on the parameters of lung function and body fat distribution as measured by DXA.

In the present study a significant reduction in BMI was found after using the IGB for 6 months (p = 0.0001). Because the risk of rupture of the device significantly increases after 6 months, this should be removed after this period [20]. Interestingly, it is believed that because an IGB occupies a large part of the stomach, it induces gastric fullness and early satiety, which favour the acceptability of the calorie-restricted diet prescribed during treatment, resulting in weight loss [21–23]. In addition, ghrelin production seems to be inhibited during the use of IGB, which contributes to satiety and thus to weight loss [24].

In addition to weight loss, we found significant body fat reduction in all the areas assessed by DXA after 6 months of IGB use. DXA is currently considered the gold standard for direct assessment of regional and total body fat and lean mass [8]. It is a non-invasive technique and provides reliable results with satisfactory accuracy [25]. Analysis of the regional fat distribution has paramount importance from the clinical point of view, as there are various phenotypes of obesity [26]. Interestingly, abdominal fat deposition is directly correlated with insulin resistance and other metabolic disorders, such as diabetes [27]. IGBs are also effective in the improvement of MS parameters [28, 29]. Crea et al. [30] reported improvement of MS parameters after 1 year of IGB use. Our study corroborates their results, as all the MS parameters improved. These results are worth emphasising because MS increases the risk of morbidity, cardiovascular disease in particular [31]. Several hypotheses have been formulated to account for the development of MS and its complications. The hypothesis that is currently most widely accepted suggests that a dysfunction of the adipose tissue alters the metabolism of free fatty acids and the release of adipokines, resulting in an inflammatory state and insulin resistance [32, 33].

Obesity alters the respiratory mechanics, thereby increasing the oxygen consumption. Lazarus et al. [34] showed that central fat deposition exerts a considerable impact on diaphragm mobility and modifies the lung volumes. In this regard, in obese individuals, the amount of abdominal fat was negatively correlated with chest wall compliance [35–37]. Additionally, Dixon et al. [38] emphasised the effects of obesity on lung function, observing that the impairment of the respiratory system function is not only due to the mechanical effects of fat deposition. In fact, the mediators produced by adipose tissue, i.e. the adipokines, also play important roles in lung tissue physiology. Medoff [39] and Konter et al. [40] investigated the effects of adipokines on the alveolar-capillary membrane and lung blood vessels and showed that they induce a pro-inflammatory state in the lung that contributes to lung damage in obesity. In the present study, FRC increased considerably after the use of IGB, and TLC, ERV, and ERV significantly increased. These results show that obesity has a tendency to induce restrictive disorder, which improves with the use of IGB [9].

The present study found a significant correlation between TLC and WC. These results further support the role attributed to abdominal fat in the development of restrictive disorder and its deleterious influence on ventilatory mechanics [41]. WC is related to the intra-abdominal and subcutaneous adipose tissue, and it seems to be a better indicator of intra-abdominal fat than BMI [42]. Therefore, elevated WC might be a predictor of restrictive defect in patients with MS. Our investigation also found significant correlations between delta FRC and delta BMI and between delta ERV and delta BMI. These results suggest that the BMI reduction induced by IGB was accompanied by increased FRC, most likely due to elevation of ERV. A reduced FRC is one of the main deleterious effects of obesity on lung function [34, 43–45]. Nevertheless, to the best of our knowledge, the present study is the first to show that the use of IGB in the treatment of obesity promotes a similar effect.

We also found significant correlations between the change in ERV and the changes in truncal, android, gynoid, and total fat. As mentioned above, fat deposition is one of the main mechanisms behind lung function impairment in obese people, particularly via reduction of ERV [43], suggesting that the progressive changes in ERV might be considered a ‘biomarker’ of the modifications that occur in the body composition during the use of IGB. Reduction of the trunk (truncal) or abdominal (android) fat was not the only finding that influenced the changes in ERV; in a separate analysis, the reduction of the fat percentage in the gynoid pattern exhibited a significant correlation with delta ERV. These results strengthen the hypothesis that the direct action of fat on respiratory mechanics is not the only cause of lung function impairment in obesity. It is likely that this correlation is also influenced by hormonal effects.

Our study has some limitations. First, it lacked a control group that did not receive an IGB, and the consistency of the results might have been enhanced by comparison with other weight loss methods. Second, DXA does not allow for a distinction between subcutaneous and visceral fat, which might have allowed for a more thorough analysis of the role of each type of fat in the present study. Third, the assessment ended upon removal of IGB. Future studies might assess these same outcomes after IGB removal. In spite of these limitations, we believe that our study represents an important contribution to this field, as no previous study has assessed the changes in lung function induced by IGB.

To conclude, the present study showed that the use of IGB in obese or overweight patients with MS promoted improvements of lung function parameters. In addition, IGB improved MS parameters as well as body composition as assessed by DXA. Therefore, the use of IGB was efficacious in inducing weight loss and simultaneous global improvement of the patients’ state of health.