1 Introduction

Rheumatoid arthritis (RA) is a systemic autoimmune disease characterized by inflammatory arthritis and extra-articular involvement [1]. RA affects approximately 0.5–2% of the world's population; RA most frequently affects people between the ages of 25 and 55 and is more common in women (2.5:1) [2].

A variety of extra-articular presentations of the disease are observed in approximately 50% of RA patients [3, 4]. Pulmonary involvement is common in RA and is the most severe extra-articular involvement, affecting 20–67% of patients and accounting for approximately 10–20% of mortality in RA patients [3]. Pleural involvement is typically asymptomatic because clinical symptoms are less common than histological changes, causing limitations that make physical activity difficult. Respiratory involvement may be asymptomatic, but the mortality rate from pulmonary disease in patients with RA is twice that of the general population [5]. Chest pain, coughing, and dyspnea are rarely reported by patients. These latter signs and symptoms may be due to concurrent pulmonary involvement [6, 7].

Pulmonary function tests are most commonly used in clinical practice to determine prognosis, monitor disease progression or treatment response, identify adverse drug reactions, and assess functional impairment or decline [7, 8]. As the majority of RA patients are asymptomatic for long periods, widely available spirometry can be used to screen and monitor RA patients for early diagnosis of PFT abnormalities, thus facilitating early intervention [3, 9]. According to a study using pulmonary function tests and lung diffusion capacity for carbon monoxide, up to 41% of patients with rheumatoid arthritis had interstitial lung involvement, but this percentage increased to 65% when high-resolution computed tomography of the chest was used for diagnosis [10].

Interstitial lung disease has been associated with risk factors such as advanced age, male sex, and a history of cigarette smoking. The PFTs of these individuals show abnormalities in diffusion and restrictive patterns [10]. According to several studies, severe restrictive [9, 11, 12] and/or obstructive PFT patterns [9, 13] have been associated with long-term RA. According to Biomdo et al., 38.5% of patients had impaired lung function, as determined by spirometry. Obstructive patterns accounted for 20.4% of all ventilatory defects, followed by restrictive patterns at 16.8% and combined obstructive and restrictive ventilatory defects at 1.2% each [14].

In a case‒control study of 40 people with RA and 60 healthy people, nine patients had a restrictive pattern on lung function tests, while one patient had an obstructive pattern. The mean FVC, FEV1, and FEV1/FVC ratios were all significantly lower in the disease group than in the control group [12]. Another study focusing on RA patients without pulmonary symptoms revealed that the FEV1:FVC ratio differed significantly between RA patients and healthy subjects and that the FEV1% and FVC% were significantly lower in RA patients than in healthy subjects [15].

There is debate concerning the pattern of ventilatory dysfunction in RA patients, with numerous studies yielding conflicting findings [9,10,11,12,13,14,15]. It is also unknown how long RA has existed and how active the disease has been in the lungs. A crucial problem that requires additional investigation is the advantage of using PFTs as a screening tool for lung involvement in RA patients. The purpose of this study was to assess how RA affects PFTs in Sudanese RA patients who visited rheumatology clinics at Omdurman Military Hospital.

2 Methods

2.1 Study design

This was an analytical, cross-sectional, community-based study conducted in the Rheumatology Unit, Outpatient Department, Omdurman Military Hospital, Omdurman City, Sudan.

2.2 Study area

The Omdurman Military Hospital is located within 15 kilos from the Khartoum Center. Omdurman Military Hospital has referral units specializing in rheumatology, and patients from all states of Sudan attend them for treatment. Rheumatology units are composed of consultants in rheumatology and are regarded as the main reference rheumatology clinic for the majority of patients with RA in Sudan.

2.3 Study population

This study included 32 patients with proven RA diagnosed according to the 2010 RA ACR/EULAR criteria of the American College of Rheumatology [16].

2.3.1 Inclusion criteria

  • The ages of the included RA patients ranged from 20–60 years

  • The subjects for the study were selected based on the 2010 RA ACR/EULAR criteria [16].

2.3.2 Exclusion criteria

  • Pregnant patients

  • Subjects with respiratory illness (asthma, COPD, pulmonary fibrosis, tuberculosis, and others)

  • Smokers

  • Diabetic subjects

  • Cancers and hematological disease patients

  • Patients on radiotherapy or chemotherapy

  • Previous chest or abdominal surgery

  • Subjects with CVD or coronary artery disease

  • Subjects with thoracic or vertebral abnormalities

2.3.3 Sampling method

For individuals who consented to participate in this research, total coverage sampling was used. The formula for calculating sample size was n = Z(2) * P(P-1)/d(2). (where n is the sample size, Z is the confidence level (interval) up to 95%, P is the predicted prevalence from early research, d is the precision (error margin) of 5%, and P is the population) [17].

2.4 Data collection

The questionnaire used in this study was composed of four sections, and all sections were developed by the authors except for section two, which was adopted from the 2010 RA ACR/EULAR criteria {16}. The questionnaire collected demographic data, social habits, RA duration and diagnosis, respiratory symptoms, extra-articular symptoms and medication history. The questionnaire is provided in Additional file 1.

2.5 Physical examination

Anthropometric measurements and assessments of lung function were performed on all study participants. Height and weight were measured, and body mass index (BMI) was calculated as weight (kg)/height (m2).

2.6 Pulmonary function test measurements

Pulmonary function tests were performed using an electronic digital spirometer (pocket microspirometer, VIASYS Healthcare GmbH, D-97204 Hoechberg, Germany) according to a standardized method [18]. The subject in a seated position was instructed to inhale maximally and rapidly with a pause of ≤ 2 s at TLC and then to exhale forcefully into the mouthpiece of the spirometer with maximal effort until no more air could be expelled while maintaining an upright posture. The FEV1, FVC, FEV1/FVC ratio, and PEFR were recorded. Three readings were taken for each subject, and the best of the three reproducible test results was recorded. The PFT results for each participant were compared with Sudanese adult spirometric reference values matched for sex, age and height [19].

2.7 Data analysis

The data were analyzed using SPSS software, version 25. A sample t test was used to compare the results of the PFTs with the Sudanese spirometric reference values. Correlations were measured using Person correlation (r), and a P value ≤ 0.05 was considered to indicate statistical significance.

3 Results

3.1 Demographic data

Thirty-two Sudanese RA patients were included in this study. Thirty-two females were included in the study. Their ages ranged from 24 to 60 years, and the mean age was 44.6 ± 11.4 years. The mean BMI was 27±6.1. Table 1

Table 1 Anthropometric measurements of the RA patients. (n = 32)
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3.2 Duration of RA

A total of 46.9% (15 patients) had been diagnosed with RA for 1–5 years, 37.5% (12 patients) for 5–10 years, and 15.6% (5 patients) for more than 10 years.

3.3 PFTs among RA patients

The mean values of FEV1, FVC, FEV1/FVC%, and PRFR in RA patients were 1.8 ± 0.3 L/min, 2.1 ± 0.4 L/min, 87.1 ± 12.2% and 223.6 ± 86.2 L/min, respectively.

The FEV1, FVC, FEV1/FVC%, and PEFR of the RA patients were significantly lower than the control reference values, as shown in Table 2 and Fig. 1.

Table 2 Comparisons of PFT parameters between RA patients and patients with matched Sudanese reference values [19]
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Fig. 1
figure 1

Comparison between the FEV1 and FVC of RA patients and matched Sudanese reference values [19]

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3.4 Correlations and associations of PFT scores with age, BMI and duration of RA

No statistical significance was observed when comparing PFT with age, BMI, or disease duration, as shown in Tables 3 and 4.

Table 3 Correlations of PFT parameters with age and BMI
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Table 4 Comparison of PFT parameters according to age, duration of RA, and BMI
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3.5 Patterns of respiratory defects among RA patients

Only 2 RA patients (6.2%) had normal PFT parameters, and 30 patients (93.8%) had abnormal PFTs. Five patients (15.7%) had an FEV1/FVC < 75%, indicating an obstructive lung defect. In twenty-five patients (78.1%), the FEV1/FVC ratio was ≥ 75%, indicating restrictive defect abnormalities in asymptomatic rheumatoid patients, as shown in Fig. 2.

Fig. 2
figure 2

Pattern of ventilation among RA patients (n = 32)

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Table 5 shows the pattern of ventilation in RA patients according to age, BMI, and duration of RA.

Table 5 Effect of RA on FEV1/FVC across different categories (n = 32)
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4 Discussion

Spirometry is the most common and most useful lung function test. This finding has extensive clinical implications. It is the least expensive test to perform, and it should be the test most widely available in doctors’ offices, clinics and hospitals. One of the common extraarticular organs involved in RA is the lung. Pulmonary dysfunction in RA is associated with a poor prognosis. In this study, in Omdurman, Sudan, RA patients were the subject of an analytical cross-sectional community-based study from August to September 2022. This study aimed to assess the pulmonary function of Sudanese RA patients meeting the 2010 RA ACR/EULAR criteria [16] and compare them with those of patients with normal Sudanese values [19]. Patients with respiratory signs and symptoms, smokers, diabetic patients [20] and those with established respiratory disease were also excluded from the study.

In this study of 32 RA patients, only 2 RA patients (6.2%) had normal PFT parameters, and 30 patients (93.8%) had abnormal PFTs. Five patients (15.7%) had an FEV1/FVC < 75%, indicating an obstructive lung defect. In twenty-five patients (78.1%), the FEV1/FVC ratio was ≥ 75%, indicating restrictive defect abnormalities in asymptomatic rheumatoid patients.

According to the results of the study, there were more female RA patients than male patients over the same period, with a ratio as high as 32:1, and no males were included in this study. However, this is slightly greater than what has been reported in other populations [21].

According to the results of the study, the mean age was 44.6 ± 11.4 years, which is comparable to the findings of the S. Padma Priya study [22].

The FEV1, FVC, and PEFR were significantly lower in the RA patients than in the controls. These findings were observed in RA patients who had no pulmonary symptoms or indicators. As a result, this study demonstrated early pulmonary deterioration in patients with silent rheumatoid lung disease and the value of PFTs in identifying patients who need to be monitored.

Regarding the pulmonary function test parameters, the mean values of FVC, FEV1, and PRFR were found to be significantly lower than those of the control group of normal Sudanese individuals derived from the study of Bashir et al. [19]. The results of our study are in accordance with the findings of Mohd Noor et al. [23], Sheianove et al. [24], Pappas et al. [25], and Bongartze et al. [26], who reported a decrease in both FEV1 and FVC% in patients with RA.

In this study, the FEV1/FVC ratio was found to be normal, and no significant differences were reported compared to those in the control group. This is expected if the abnormality affects both FEV1 and FVC. This finding was inconsistent with one study that reported a significant difference in the FEV1/FVC ratio between RA patients and healthy subjects {15}.

Obstructive ventilatory defects are observed in 15.7% (5) of rheumatoid patients with an FEV1/FVC < 75%, where the FEV1 is reduced more than the FVC. Restrictive ventilatory defects are observed in 78.1% (25) of rheumatoid patients with FEV1/FVC > 75, where both FEV1 and FVC are reduced. Obstructive, restrictive, and mixed patterns of lung involvement have been documented in RA patients by Biomdo et al. {14}, Bilgici et al. {27}, and Habibet al. [28], which is similar to the results of our study.

In our study, we found that pulmonary function abnormalities, mainly restrictive abnormalities, are common in asymptomatic rheumatoid patients. This result, in agreement with a 5-year prospective study performed by Avnon et al. [29], revealed a significant decline in pulmonary function, and they noted small airway obstruction as well as a restrictive pattern in RA patients. These findings agree with other studies, such as those of Haithem J. Kadhum [11], Pappas et al. [25], Hyland et al. [30], and Cavagna et al. [31], which also revealed a restrictive pattern in RA patients. Gowdhaman et al. [32] also reported a restrictive type with a decrease in vital capacity.

Additionally, our findings were not similar to those of a study that included RA patients without pulmonary symptoms, showing that there was a significant difference in the FEV1/FVC ratio between RA patients and healthy individuals {15}, as we found a normal FEV1/FVC ratio in our study.

The activation of immune complexes in alveolar walls may be the cause of restrictive ventilatory dysfunction in RA patients. This results in the release of collagenase, elastase, and myeloperoxidase. Phagocytosis leads to the loss of lung tissue, and an imbalance between protease and antiprotease activity limits lung expansion [5].

According to Cortet et al. [33] and Radoux et al. [34], obstructive lung disease was found in 50% of patients, with a decrease in FEV1 of 25–75%. The prevalence was lower in our sample, where only 15.7% of the RA patients had obstructive lung disease. These results contrast with those of other studies, such as those by Bilgiciet et al. [27], Cortetet et al. [35], Perez et al. [36], and Collins et al. [37], which showed that an obstructive pattern was the primary lung impairment in a cohort of RA patients.

In this study, the PEFR was significantly affected in RA patients compared to their matched controls. This is in contrast to a study by Biswajit et al., who reported no significant changes or a normal PEFR in approximately 86% of patients [11].

Numerous studies, including those by Gochuico et al. [38], Fuld et al. [39], and S. Madhavan et al. [40], have shown that the duration of RA does not increase the incidence of pulmonary involvement. This finding is consistent with our study, which revealed that there was no discernible association between RA duration and PFTs. This finding is also consistent with the findings of Avnon et al. [29] and S. Padma et al. [22]. However, other studies have shown that the duration of RA influences the rate at which lung involvement develops [9, 11,12,13, 22, 41].

In addition, our study revealed no statistically significant associations between PFTs and age or BMI. In line with our findings, the study by S. Madhavan et al. revealed no association between age and outcome [40].

This study has several novelties; in previous studies, there is debate concerning the pattern of ventilatory dysfunction in RA patients, with numerous studies yielding conflicting findings. Based on our findings, we recommend updating RA management and guidelines by suggesting frequent spirometry testing as a baseline and follow-up and promoting early detection and management of pulmonary involvement in RA patients. On the other hand, this is the first study in Sudan to investigate how RA affects PFTs in Sudanese RA patients.

This study had several limitations. First, because it was cross-sectional, no patients were followed up, and second, PFTs are not the only reliable method for identifying respiratory disease. As PFTs are common and low-risk diagnostic methods that are often used in clinical practice before radiography, we decided to use PFTs as a marker of lung disease. Longitudinal studies are needed to determine how treatment affects these abnormalities. Additionally, the adherence to medications and the effects of the use of different and multiple RA drugs on PFTs were not addressed.

Furthermore, rheumatoid factor (RF) and anti-citrullinated peptide (CCP) antibody levels, radiographic changes, and diffusing lung capacity for carbon monoxide (DLCO) were not used as indicators of the severity of airway membrane involvement to determine the relationship between disease activity and lung involvement.

5 Conclusions

Unexpectedly high rates of pulmonary dysfunction were observed in the study participants, suggesting that all RA patients should undergo PFTs for a thorough evaluation. PFTs are recommended for RA patients as a baseline evaluation and for follow-up to improve early detection and management of pulmonary involvement. Patients with RA may have different patterns of lung function impairment, with a restrictive pattern being the most common.