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Novel Approaches for the Treatment of Pulmonary Tuberculosis pharmaceutics Review Novel Approaches for the Treatment of Pulmonary Tuberculosis 1, 1, 2,3, 4,5 Zhi Ming Tan y , Gui Ping Lai y , Manisha Pandey * , Teerapol Srichana , Mallikarjuna Rao Pichika 3,6, Bapi Gorain 7,8, Subrat Kumar Bhattamishra 9 2,3, , and Hira Choudhury * z 1 School of Pharmacy, International Medical University, Kuala Lumpur 57000, Malaysia; [email protected] (Z.M.T.); [email protected] (G.P.L.) 2 Department of Pharmaceutical Technology, School of Pharmacy, International Medical University, Jalan Jalil Perkasa, Bukit Jalil, Kuala Lumpur 57000, Malaysia 3 Centre for Bioactive Molecules and Drug Delivery, Institute for Research, Development and Innovation, International Medical University, Kuala Lumpur 57000, Malaysia; [email protected] 4 Drug Delivery System Excellence Center, Prince of Songkla University, Songkhla 90110, Thailand; [email protected] 5 Department of Pharmaceutical Technology, Faculty of Pharmaceutical Sciences, Prince of Songkla University, Songkhla 90110, Thailand 6 Department of Pharmaceutical Chemistry, School of Pharmacy, International Medical University, Kuala Lumpur 57000, Malaysia 7 School of Pharmacy, Faculty of Health and Medical Sciences, Taylor’s University, Subang Jaya, Selangor 47500, Malaysia; [email protected] 8 Centre for Drug Delivery and Molecular Pharmacology, Faculty of Health and Medical Sciences, Taylor’s University, Subang Jaya, Selangor 47500, Malaysia 9 Department of Life Science, School of Pharmacy, International Medical University, Jalan Jalil Perkasa, Bukit Jalil, Kuala Lumpur 57000, Malaysia; [email protected] * Correspondence: [email protected] (M.P.); [email protected] (H.C.) The authors contributed equally in this article. y This author is the main Correspondence author. z Received: 20 October 2020; Accepted: 1 December 2020; Published: 10 December 2020 Abstract: Tuberculosis (TB) is a contagious airborne disease caused by Mycobacterium tuberculosis, which primarily affects human lungs. The progression of drug-susceptible TB to drug-resistant strains, MDR-TB and XDR-TB, has become worldwide challenge in eliminating TB. The limitations of conventional TB treatment including frequent dosing and prolonged treatment, which results in patient’s noncompliance to the treatment because of treatment-related adverse effects. The non-invasive pulmonary drug administration provides the advantages of targeted-site delivery and avoids first-pass metabolism, which reduced the dose requirement and systemic adverse effects of the therapeutics. With the modification of the drugs with advanced carriers, the formulations may possess sustained released property, which helps in reducing the dosing frequency and enhanced patients’ compliances. The dry powder inhaler formulation is easy to handle and storage as it is relatively stable compared to liquids and suspension. This review mainly highlights the aerosolization properties of dry powder inhalable formulations with different anti-TB agents to understand and estimate the deposition manner of the drug in the lungs. Moreover, the safety profile of the novel dry powder inhaler formulations has been discussed. The results of the studies demonstrated that dry powder inhaler formulation has the potential in enhancing treatment efficacy. Keywords: tuberculosis; lung physiology; barriers of pulmonary delivery; advanced drug delivery; lung delivery; metered-dose inhaler; proliposome Pharmaceutics 2020, 12, 1196; doi:10.3390/pharmaceutics12121196 www.mdpi.com/journal/pharmaceutics Pharmaceutics 2020, 12, 1196 2 of 54 1. Introduction Tuberculosis (TB) is one of the major health concerns in the world, with at least 10 million people being infected each year [1]. It is a contagious airborne disease caused by Mycobacterium tuberculosis, which is transmitted from person-to-person via the air droplets. M. tuberculosis is primarily affecting the lungs causing pulmonary tuberculosis, but it can also adversely affect intestine, bones, joints, and other tissues of the body causing extra-pulmonary tuberculosis. TB can be classified into two groups, which are latent TB and active TB. People with latent TB show asymptomatic and is not transmissible while people with active TB show noticeable symptoms and the disease can spread to others [1,2]. All age groups are at risk of getting affected by TB, however, people with immunodeficiency virus (HIV) infection and suffering from other disease conditions that impair the immune system are at higher risk of developing active TB. According to the World Health Organization (WHO), tuberculosis remains one of the leading causes of death from a single infectious disease agent, including people living with HIV [1]. In 2018, it was estimated globally that 10 million people (5.7 men, 3.2 women, and 1.1 children) were affected by TB with approximately 1.5 million people died from the incidence based on the data reported by WHO [1]. As compared to previous years, there was estimated 1.6% decline in the average TB incidence rate per year from 2000 until 2018, and 2% between 2017 and 2018. The number of TB deaths were reduced by 11% between 2015 and 2018 [1]. One of the greatest obstacles in controlling TB is the emergence of drug-resistant tuberculosis. There are two types of drug-resistant tuberculosis namely: multidrug-resistant tuberculosis (MDR-TB) and extensively drug-resistant TB (XDR-TB). In the case of MDR-TB, the two most potent first-line anti-TB drugs, isoniazid (INH), and rifampicin (RIF) are reported ineffective in treating TB as the TB bacteria are resistant to those drugs. The emergence of MDR-TB is mainly due to the inappropriate use of anti-TB drugs, poor quality of anti-TB drugs, wrong prescription by healthcare providers and premature interruption of the treatment. XDR-TB is a more severe form of drug-resistant TB caused by ineffective management of MDR-TB [3,4]. Additionally, XDR-TB is a form of MDR-TB with additional resistance to any fluoroquinolone and at least one of the three injectable second-line anti-TB drugs (amikacin, kanamycin, or capreomycin). In 2018, there were estimated 484,000 new cases of MDR-TB which was resistant to RIF. About 78% of people developed MDR-TB meanwhile 6.2% of people from MDR-TB had XDR-TB as reported by WHO [1]. The standard TB treatment is to strictly follow six months of drug regimen provided with patient support and supervision. As a simple reason, the inappropriate management of TB and inadequate adherence to the treatment can result in the continuing spread of drug-resistant TB [5]. Drug-resistant TB is mainly attributed to a mutation in the targeted genes of antibiotics due to previous improper treatment of TB. As a result, the TB bacteria evolve to become more resistant to the prescribed antibiotics [6]. In addition to targeted gene alteration, a decrease in the permeability of the TB bacteria cell wall inhibits the entry of antibiotics into the cell. Consequently, the accumulated antibiotics are degraded slowly by enzymes released from the bacterial cells. Based on the report by Almeida et al., M. tuberculosis produces an enzyme called β-lactamase that can degrade β-lactam antibiotics which leads to the resistance of the bacterial towards the respective antibiotics [7]. Besides this, the efflux pump in M. tuberculosis can pump the antibiotics out of the bacterial cells which also leads to drug resistance (Figure1)[ 8,9]. The treatment for drug-resistant TB requires a longer period to complete and is manageable by second-line anti-TB drugs such as fluoroquinolones, kanamycin, linezolid, bedaquiline, cycloserine and pretomanid. However, the availability of second-line anti-TB drugs is complex and most exhibit several systemic toxic effects such as irreversible ototoxicity, hepatotoxicity, hyperpigmentation and bone marrow toxicity [4,10]. Pharmaceutics 2020, 12, 1196 3 of 54 Pharmaceutics 2020, 12, x FOR PEER REVIEW 3 of 60 Figure 1. Bacterial antibiotic resistance mechanisms in drug-resistant TB. Mechanisms of bacterial antibiotic resistance include altera alterationtion in the drug-targeted genes; decreased permeability of the TB bacteria cellcell wallwall which which inhibits inhibits the the entry entry of antibiotics;of antibiotics; degradation degradation of antibiotics of antibiotics by enzymatic by enzymatic action; action;loss/altered loss/altered in the drug in the entry drug port; entry expression port; expr ofession efflux of pumps efflux pumps on thecell on the membrane. cell membrane. 2. History History of of Treatments Treatments of TB and Associated Limitations TB has been called “phthisis” (ancient Greece), “tabes” (ancient Rome), Rome), and and “schachepheth” “schachepheth” (ancient Hebrew)Hebrew) [11[11,12].,12]. InIn 17th 17th and and 18th 18th centuries, centuries, the the term term “consumption” “consumption” was was commonly commonly used used as a aslay a termlay term for phthisis for phthisis [12]. [12]. In 1834, In 1834, the termthe term “tuberculosis” “tuberculosis” was was coined coined by Johann by Johann Lukas Lukas Schönlein Schönlein [11]. [11].TB was TB awas lethal a lethal disease disease with no with cure no until cure the until cause the of cause TB was of revealed.TB was revealed. The discovery The discovery of TB treatment of TB treatmentin the 20th in century the 20th remains century one remains of the greatestone of the achievements greatest achievements in human history. in human In 1882, history. Robert In Koch1882, Roberthad discovered Koch had the discovered cause
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