The global burden of pulmonary fungal infections caused by opportunistic fungal pathogens is increasing [19]. Sustaining of patients by drugs, chemicals, and mechanical processes that compromise physical barriers to infection, suppress immune mechanisms, or upset the balance of normal flora are responsible for rendering hosts more susceptible not only to pathogenic fungi but also to all fungi with which they come in contact. The increased age of the world population that resulted in more chronic diseases with their debilitating effects is also another attributing factor for an increase in fungal lung infection by opportunistic fungal pathogen [20]. The impact of these factors may explain for the higher prevalence of fungal pulmonary infection reported in the present study.
The present study revealed that the prevalence of PTB, pulmonary fungal pathogens and PTB-fungal pathogen co-infection were found out to be 25.6%, 75.9%, and 20.0%, respectively. Our result regarding the prevalence of PTB and pulmonary fungal pathogens was consistent with the findings of Sani et al [21] but PTB- fungal pathogen co-infection in our study was three-fold (20.0% against 6%) from that of their report. On the other hand, PTB fungal coinfection in the range of 18–40% was reported by other similar studies [22, 23]. Among 163 study subjects that were positive for M. tuberculosis, 123 (77.9%) were co-infected with fungal pathogens. The high prevalence of PTB fungal pathogen co-infection in study subjects with tuberculosis in our study may support that pre-existing or residual cavity produced following tuberculosis infection are frequent places of fungal colonization and the chromic nature of PTB along with prolonged chemotherapy makes PTB patients more susceptible to fungal infection [4]. The high prevalence of PTB and fungal co-infection exhibited in this study may worsen the existing burden of PTB and, hence, due attention should be given.
Lower respiratory tract fungal infection (pulmonary mycosis) such as aspergillosis frequently occurs in middle-aged to an elderly individual, and are more commonly reported in male patients [24, 25]. Our finding was in line with the findings of Kosmidis and Denning [24] and Kohno et al [25] as the isolation rate of fungal pathogens was higher in patients above 35 years than younger age groups and male than female study participants. Other studies [26, 27], however, demonstrated that the age group of 20–34 years is most affected by fungal pathogens. Certainly, old age is a known risk factor for pulmonary fungal infection probably due to diminishing immune function as one gets aged [20]. The association of pulmonary fungal infection with age and sex in our study was not statistically significant with respective P- values of 0.239 and 0.50.
In the present study, of a total of 636 sputum cultures, 483 were positive for fungal pathogen and a total of 690 fungal isolates were recovered. Furthermore, out of 483 positive culture, 43 samples yielded more than one fungal species. Among the isolates, 562 were yeasts where NAC species comprised the most predominant yeast isolates (52.7%). At the species level, however, C. albicans was the most prevalent species accounting for 46.2% yeast isolates. This was followed by C. tropicalis and C. krusei. Numerous studies have reported that Candida species are the most frequent fungal species recovered from the sputum of patients with pulmonary tuberculosis [24, 25, 28, 29].
Even though Candida species were noted as the most frequent fungal species recovered from the sputum of patients with tuberculosis its significance has always been a matter of debate because up to 32.5% of healthy individuals harbor Candida in their throat that can contaminate the sputum during sample collection [30]. Correspondingly, our study depicted that C. albicans was the most prevalent yeast in PTB yeast co-infected patients accounting for 64.6% of yeast isolates. Similar other several studies [31–33] demonstrated a high prevalence isolation rate of C. albicans ranging from 45–92% in PTB patients co-infected with yeasts. The existence of candidiasis concurrently with PTB patients is of paramount interest in the treatment of patients as C. albicans is supposed to enhance the virulence of PTB [22]. Although C. albicans continues to be the most predominant species in pulmonary candidiasis [31–33], several NAC species are also reported in increasing frequency. C. tropicalis and C. krusei were isolated as the 2nd and the 3rd most prevalent yeasts in PTB-yeast co-infected patients with respective frequencies of 22.6% and 19.9%. our result is in line with Latha et al [31], Jain et al [32], and Baradkar et al [33]. C. tropicalis is an emerging pathogen with higher rates of severe disease and deep tissue invasion than C. albicans in immune- debilitated individuals, and C. krusei is noted as intrinsically resistant emerging yeast pathogen to azole antifungal drugs particularly to that of fluconazole [34, 35].
Fungal infections of the respiratory tract by large are considered to be identical with invasive pulmonary infections caused by Aspergillus SPP.[6]. Our finding was consistent with this report because out of 128 mycelial fungi recovered in the present study 61.7% (79) of the isolates were Aspergillus species. Among a hundred species of Aspergillus, A. fumigatus, A. flavus, A. niger, and A. terreus are pathogenic species to man. Most previous studies reported that A. fumigatus is the most common cause of chronic-pulmonary aspergillosis [21, 36–38], although its incidence appears to be decreasing in recent years with an increase in cases by other no-fumigatus species, especially A. flavus, A. niger, and A. terreus [39]. In the present study, A. niger was the most frequently isolated Aspergillus species followed by A. fumigatus and A. flavus. Our finding was in line with the findings of Park et al [40]. According to Park et al [40], non-fumigatus Aspergillus species are known to cause all forms of aspergillosis. Correspondingly, our study depicted that Aspergillus species were the most prevalent mycelial fungi in PTB mold co-infected accounting for 14.96% of mold isolates.
Pulmonary fungal infections have long been recognized as a significant complication and mainly caused by C. albicans and Aspergillus SPP. Within the past few decades, however, infections due to infrequently encountered fungi (e.g., Penicillium SPP., Scedosporium SPP., dematiaceous filamentous fungi, and zygomycetes) have become increasingly common in immunocompromised hosts [6]. Our finding supports the report of Chowdhary et al [6] in that the isolation rate of mycelial fungi other than Aspergillus SPP. was considerable. Among 128 mycelial fungi isolated 49 (38.3%) were mycelial fungi other than Aspergillus SPP. Among non-Aspergillus isolates, 16(12.5%) were represented by Penicillium SPP. of which 5(31.25%) of the isolates were P. marneffei and the remaining 11(68.75%) were other Penicillium SPP. P. marneffei is an emerging dimorphic fungal agent that can cause a deadly systemic mycosis in subjects infected with human immunodeficiency virus [41] while Penicillium SPP. other than Penicillium marneffei have been recovered most frequently in the clinical laboratory as culture contaminants. They have, however, been emerged as opportunistic pathogens in an immunocompromised individual and consequently, it should not be regarded as a contaminant without a thorough investigation [42].
In our study, S. apiospermum and Fusarium SPP. accounted for 10.2%;13 and 7.8%;10 of the isolates of mycelial fungi, respectively. S. apiospermum is among the most common filamentous fungi colonizing the lungs of cystic fibrosis patients with a frequency of 9% [43]. Fusarium species once considered to be important plant pathogens are known to cause a broad spectrum of infections including mycotic keratitis and onychomycosis. Lung involvement is common in invasive fusariosis occurring among immunocompromised patients with disseminated infection [44]. Species of Alternaria, Bipolaris, Curvularia, and Exserohilum have been reported to cause different types of human respiratory tract infections including invasive lung disease [Chowdhary [6, 45, 46]. Isolation of Alternaria and Bipolaris species in our study supports the findings of Chowdhary et al [6], Bush and Prochnau [45], and Chowdhary et al [46].