INTRODUCTION

Tuberculosis (TB) is a chronic infectious disease, caused by a mycobacterium, mainly affecting the lungs and consequent extrapulmonary involvement, such as the larynx ^1,2. Incidentally, laryngeal tuberculosis (LTB) can become the first clinical manifestation of pulmonary tuberculosis ^1,2,3. At present, LTB is an uncommon manifestation of TB, being the most frequent disease that affects the larynx, which represents 1% of the cases ^4,5,6, due to the fact that there are no concrete characteristics of this disease ⁷, since the clinical models are constantly changing ^8,9,10 because this disease can be located both in the posterior larynx (arytenoid cartilage) and, more frequently, in the anterior part of the larynx (vocal folds and epiglottis), therefore, making it difficult to diagnose and even to the point of being confused with other diseases, such as fungal laryngitis, syphilis, Wegener's granulomatisis, and sarcoidosis ^8,9,11,12,13.

All cases of LTB can have major epidemiological consequences ¹⁴, if not detected in time, as it is considered a highly contagious disease ¹⁵. According to WHO, TB has been declared a global epidemiological emergency, since a large part of the world's population is exposed to contact with the mycobacterium, where 1 in 10 people may develop this disease at some point in their lives ^16,17. LTB has been one of the most common and prevalent health problems, although, in recent years, ¹⁸ the number of TB cases has been reduced, however, the decrease has not been as significant ¹⁹. According to WHO, by mid-2021, 1.6 million people died from this disease ^20,8. TB in China averages 0.0036%, equivalent to 4.5 million patients with active pulmonary TB and 1.5 million new infections per year ^21,22, followed by Russia, with an average of 0.3-1.4% ^23,24,25. According to studies, men are four times more likely to be affected than women ^21,26, with the vocal folds being the main site with the greatest lesion, as they are the oscillatory mechanism for producing the voice ²².

LTB involvement ²⁷ can develop most frequently through bronchogenic ²⁸, hematogenous or lymphatic spread of lung disease, on the other hand, it can also develop through direct invasion of the larynx by inhalation ^9,22,29. LTB infection ³⁰ can cause irreversible changes in the vocal folds, together with alterations in the epiglottis, anterior and posterior commissure, vestibular and aryepiglottic folds, causing dysphonia as the main effect ^4,31. On the other hand, effects such as hoarseness, cough, dysphagia, and odynophagia and weight loss are also reflected ^1,2,26,20. Furthermore, LTB is divided into four categories of videolaryngoscopic appearances ³², being mainly the granulomatous lesion, followed by ulcerative, erosive, and non-specific inflammatory lesions ^6,33,34. LTB can be difficult to treat, especially in advanced cases, and may require surgery or prolonged drug treatment ^20,35. If the person is misdiagnosed ³⁶, LTB can have serious consequences for the patient and the person with whom he or she is in contact ^9,37.

In addition, LTB ³⁸ can have a significant impact on a person's quality of life, as it can cause dysphonia, difficulty swallowing and breathing ³⁹, and LTB can leave long-term sequelae, negatively affecting the process of restoring voice quality ³¹. Considering the arguments and findings previously revealed the following research question arises: What is the long-term effect of laryngeal tuberculosis on the adult voice?

METHOD

The research methodology is descriptive in which the inquiry, collection, organization, and analysis of the scientific information established in a time window of 10 years, where it is developed taking into account the parameters of the PRISMA statement supported by the authors Brian Huttona, Ferrán Catalá-Lópeza, David Moher ⁴⁰, a tool that allowed the systematic review of the scientific literature from the identification of databases, search, and selection of research articles on LTB and its long-term effects on the voice ⁴¹. The studies were selected based on inclusion and exclusion criteria that facilitate the evaluation of the quality and reliability of the studies and eventually allow answering the research question ^42,43.

The PIO model was used to construct the research question; however, the comparison section was not applied ^44,45. This tool is used because it serves to improve the specificity and conceptual clarity of the clinical problems to be studied, as well as to perform searches with greater quality and precision, which allows for the collection of pertinent and precise data to answer the problem question ^46,47.

The classification of the quality of evidence and grading of the strength of recommendation was performed through the GRADE pro GDT system ⁴⁸.

Research Question

According to the thematic established for the research, the components of the PIO model shown in table 1 were used, resulting in the following research question: What is the long-term effect of laryngeal tuberculosis on voice quality in adults?

Inclusion and Exclusion Criteria

The present systematic review employed a comprehensive search strategy that combined key terms from the Descriptors in the Health Sciences (DECS) and Medical Subject Headings (MESH). This strategy made it possible to identify and select literature relevant to the study topic, as detailed in table 3.

Search Strategies

To carry out an exhaustive and precise search, a search strategy was designed using equations formed by key terms. These equations were constructed with the help of logical operators such as AND/OR and symbols such as "" and (). This search strategy was applied in several scientific and academic journal databases as well as open access repositories, all in English. For more details (see table 4).

Sources of Information

The information sources used in this systematic review were classified into two categories:

• Scientific and academic journal databases: PubMed, Springer Link, Taylor & Francis, Scopus, and ScienceDirect.

• Open access repositories: Scielo, Redalyc and Dialnet.

Characteristics of the Studies

In the initial phase, studies were classified considering inclusion and exclusion criteria. Priority was given to those studies that focused on laryngeal tuberculosis and its effects on the voice, as reflected in their titles. Subsequently, selected studies were reviewed to ensure that they aligned with the target population of this review, i.e., adults with laryngeal tuberculosis. Studies involving children and adolescents were excluded to maintain focus on the research topic.

Selection and Analysis

A preliminary selection of studies was made based on review of inclusion criteria, population characteristics, study type, and year of publication. An Excel registration table, designed by the authors, was then completed independently, detailing the key elements of each of the selected studies.

The process of identification, screening, eligibility assessment, and inclusion of the articles was carried out following the structure proposed by the PRISMA statement. For the analysis, the GRADE system was used, which made it possible to evaluate aspects such as the number of studies, study design, risk of bias, inconsistency, indirect evidence, imprecision, and degree of certainty of the study ⁴⁸.

RESULTS

The eligibility criteria were determined following the order established in the methodology by developing each of the phases of the PRISMA flowchart (Figure 1).

Identification Phase

A search was carried out in eight databases: five scientific and academic journal databases (PubMed, Springer Link, Taylor & Francis, Scopus, and ScienceDirect), and three open access repositories (Scielo, Redalyc, and Dialnet). This search was based on the cross-referencing of variables constructed from the keywords DECS and MESH in English. A total of 91905 articles were obtained. Subsequently, filters were applied for type of document, period, incomplete or duplicate texts, articles without access and non-compliance with the criteria. Finally, a final sample of thirty-six (36) articles was obtained and used in this review (see table 5).

Selection and Elimination Phase

The final selection of the research articles was made by preliminary reading of the titles, abstracts and then the introduction. This allowed the identification of the most relevant articles with respect to the topic under investigation, selecting 36 articles. The results for each variable crossing in English are listed below (see table 6) for the eight databases.

Within the search for the selection of articles, 9 crossings of variables in English between the different variables were used, resulting in 12 articles in PubMed, 1 article in Springer Link, 2 articles in Taylor & Francis, 17 articles in Scopus, 1 article in ScienceDirect, 1 article in Scielo and 2 articles in Dialnet, giving a total of 36 articles.

Inclusion Phase

The selection was made after reading the titles and abstracts of the articles, being analyzed in their entirety with a complete reading, applying criteria that allowed a selection, which gave an answer to the question posed. The selection corresponded to a final sample of 36 articles (see table 7).

We analyzed the outcomes of the effects of LTB on the voice (see table 10), such as dysphonia, in which 7 studies were included with low certainty, 3 studies of hoarseness were included with low certainty, 5 studies of granulomas were included with low certainty, 3 studies of ulcerative lesions were included with low certainty, 3 studies of exophytic lesions were included with low certainty, 2 studies of sore throat were included with low certainty, 1 study of exophytic lesions was included with low certainty, 3 studies with ulcerative lesions with low certainty, 3 studies with exophytic lesions with low certainty, 2 studies with sore throat with low certainty, 1 study with glottic mass with low certainty, and, finally, 1 study with cough with low certainty.

ANALYSIS AND DISCUSSION

TBL is a specific form of TB that affects the upper respiratory tract, specifically the larynx; it is an infectious disease caused by the bacterium Mycobacterium tuberculosis, which is transmitted mainly through the air when an infected person coughs, sneezes, or speaks ^1,3,12. Normally, this disease can be seen in people without the Bacillus Calmette-Guerin vaccine, who are malnourished, or in patients with AIDS, low immunity or chronic smoking ⁸. The main factors of LTB are alcohol abuse and smoking ⁸. Previously, LTB had a great decrease of cases, favoring the quality of people's voice, thanks to ant tuberculosis drugs and prevention programs worldwide ⁹. On the other hand, this disease used to affect young adults between 20 and 30 years of age and without distinction of gender, but, currently, according to studies, its prevalence lies in people between 40 and 60 years of age and can affect four times more middle-aged men than women ^21,26,57.

However, in spite of everything, LTB is still considered an uncommon manifestation of TB, as it is rarely taken into account, since the clinical signs of LTB have changed in the last decades ^5,9. This condition is equivalent to 1% of TB cases, since there are no established characteristics of this disease, due to the fact that the clinical models are constantly changing, to the point of simulating another disease or covering the main disease, as in this case, LTB by diseases such as: fungal laryngitis, syphilis, Wegener's granulomatisis, and sarcoidosis ^8,9, which delays the correct diagnosis ¹¹. It is important to take into account that this condition still occurs and continues to be one of the most frequent diseases of the larynx, affecting vocal function and the quality of life of people with TB ^26,55. According to WHO, this disease has been declared a global epidemiological emergency, since a large part of the world population is exposed to contact with the mycobacterium, where 1 out of every 10 people may develop this disease at some time in their lives ^16,17. On the other hand, it is reported that, by mid-2021, 1.6 million people died from this disease ^20,8,60.

LTB can be primary, which is caused by direct invasion of inhaled substances by bacilli ^26,29,59, and on the other hand, it can be secondary, being produced by coughing and expectoration from the tracheobronchial tree or through the bloodstream from places other than the lungs ^8,39,35. The main means of transmission is the direct contamination of pulmonary secretions with high bacillary load from contaminated sputum, passing through the posterior commissure, affecting the arytenoids, the interarytenoid space, the ventricular folds and vocal folds, and, to a lesser degree, the laryngeal surface of the epiglottis, since they are exposed to the greatest impact of sputum at the moment of coughing, characterized by the formation of granulomas ¹⁶.

Although LTB is usually a clinical manifestation of pulmonary TB, supported by the most widely accepted and most prevalent bronchogenic theory ^1,2,3, there is also a theory called hema-togenic, which is uncommon and has a lower incidence, in which cases of LTB occur without pulmonary involvement, where the bacillus is transmitted through the blood ¹⁶.

Among the findings of laryngeal biopsies, the main lesion of LTB most frequently mentioned are granulomas, followed by ulcerative lesions and nonspecific lesions ^2,6,13. However, variability is reported, exophytic lesions, edema and glottic masses can also be found ^{1,3) (21}, and in turn, these lesions are reflected in certain structures such as: the glottic region (true vocal folds, vestibular folds, anterior and posterior commissures) which is usually the most affected, followed by the supraglottic region (epiglottis, aryepiglottic folds) ^3,20,6,8,15, affecting the quality of the voice, preventing its adequate production and causing great alterations ^2,9,8,13,57.

Thus, the vocal folds are the most affected site, since the glottis is the entrance to the respiratory tract, being directly exposed to the bacilli, whether they are expelled from the lungs or inhaled from the air droplets ^51,55. In addition, sound production depends on the flexibility of the vocal folds, the correct function of the muscles involved in the production and integrity of the vocal tract tissues and the formation of waves in the mucosal layer ³¹.

These can present lesions caused by chronic cough or excessive vocalization, which causes an increased probability of bacterial invasion ^3,21,. Vocal folds present a direct relationship with voice quality, since they are the oscillatory component for voice production, therefore, they are the main site affected by LTB ^20,5. Therefore, dysphonia is the main clinical effect of LTB infection ^3,5,53, which is a disorder characterized by altered vocal quality, pitch and loudness, being one of the most common laryngological effects, and the first of many laryngeal diseases ^9,50.

Due to LTB, in the sub epithelial space, there are usually areas of scarring and fibrosis, which alter the movement of the vocal folds to close and open the glottis, altering its vibration for phonatory production, manifesting rapidly progressive dysphonia, to the point of causing aphonia in the patient ^2,6. Other effects are hoarseness, cough, sore throat, stiffness, voice change, and even paralysis of the vocal folds ^55,35,58. In the case of those who present cough; this can be variable depending on the lesions, since in certain cases the patient experiences dry laryngeal cough with a foreign body impression associated with hemoptysis ². LTB can have significant long-term effects, since the larynx is a fundamental tool for sound production and vocal quality, and if TB affects it, there can be changes and alterations in the voice that last even after the disease has been treated and cured ¹.

According to studies, voice effects such as dysphonia, hoarseness, cough, pain, and stiffness, which are caused by LTB, can begin from 1 to 3 months after the pulmonary symptoms and can last from 1 to 8 months or even in the greatest of cases up to 18 months ⁴, leaving large marks and negatively affecting voice adjustments ^31,21.

The long-term effects vary according to the individual, since the susceptibility of the host depends on the state of its specific and non-specific resistance mechanisms. This will depend on the degree of lesion that the person has in the laryngeal structures and the response they have to the antituberculosis drug, whether positive or negative ⁵⁷. In most cases, the lesions and effects produced by LTB on the voice improve, thanks to a timely and effective pharmacological and therapeutic treatment ¹, achieving a total cure of LTB, without leaving sequelae ².

However, in other cases, after the antituberculosis treatment, LTB can leave certain marks or sequelae, affecting the quality and functionality of the voice, as is the case of dysphonia, mainly because, according to the literature, dysphonia is the only effect of LTB that is resistant to rifampicin, a drug used for the treatment against TB ⁹, therefore, its prevalence is much higher, compared to the other effects ³. Next, we find hoarseness as one of the most prolonged effects, even after treatment ⁵³. In the case of the vocal folds, they may be left with diffuse scars and may be slightly swollen, but their mobility was no longer affected ¹. Normally, residual adhesions may remain after treatment, so that the voice function will not be adequate ³⁵. Usually, after starting therapy or treatment against LTB, week's later improvements in symptoms and appearances in the larynx appear, making it return to normal in several months, however, if the effects are very large and because large scars, permanent functional laryngeal damage may occur ³.

CONCLUSIONS

The most affected and most frequently mentioned structure is the vocal folds, which causes alterations in the quality and functionality of the voice. On the other hand, dysphonia is the main effect that triggers LTB, since the vocal folds present alterations in their flexibility and oscillatory function for voice production, and although there is an effective pharmacological and therapeutic treatment, which manages to eliminate 100% of the TB bacteria, and to avoid the appearance of long-term sequelae, it also often only manages to reduce the effects left by LTB, such as dysphonia and hoarseness, which are some of the main effects on the voice that can continue to remain and affect the functionality of the voice, in the case of dysphonia since it is resistant to rifampicin.

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Notes

Author notes

*Correspondencia: Diego Rivera-Porras. drivera23@cuc.edu.co