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 Table of Contents  
Year : 2022  |  Volume : 11  |  Issue : 4  |  Page : 415-422

Effect of COVID-19 pandemic on incidence of mycobacterial diseases among suspected tuberculosis pulmonary patients in Tehran, Iran

1 Mycobacteriology Research Centre, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
2 Department of Biotechnology, School of Advanced Technology in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
3 Clinical Tuberculosis and Epidemiology Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
4 Department of Global Public Health, Karolinska Institute, Stockholm, Sweden

Date of Submission07-Aug-2022
Date of Decision10-Sep-2022
Date of Acceptance22-Oct-2022
Date of Web Publication10-Dec-2022

Correspondence Address:
Poopak Farnia
Department of Biotechnology, School of Advanced Technology in Medicine, Shahid Beheshti University of Medical Sciences, Tehran
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmy.ijmy_167_22

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Background: Recent pandemic of coronavirus SARS-CoV-2 (COVID-19) caused limitations in the country's strategies to fight against mycobacterial infections. The aim of this study was to compare the suspected tuberculosis (TB) pulmonary patients before and during the COVID-19 pandemic (January 2018–December 2021) who were referred to the National Reference TB Laboratory (NRL TB), Tehran, Iran. The mycobacterial isolated strains were identified and compared with previous data. Methods: A total of 16,899 clinical samples collected from 7041 suspected pulmonary TB patients were received from 2018 to 2021. Primary isolation of Mycobacterium isolates was done on Löwenstein–Jensen medium. Then, the DNA was extracted from acid-fast bacillus culture-positive samples and identification was performed by IS6110, Hsp65, and 16S-23S rRNA genes using polymerase chain reaction (PCR), PCR-restriction fragment length polymorphism, and nested PCR methods. Results: A total of 11679 specimens (69.1%) from 4866 suspected TB patients were collected in 2018–2019 and 5220 specimens (30.8%; from 2175 patients) in 2020–2021. Out of 11679 specimens, 2046 samples that belong to 852 patients were infected with Mycobacterium tuberculosis, and the remaining were non-TB Mycobacterium (NTM) species (n = 244) isolated from 102 patients. The cultures for 12894 specimens were either negative (76.3%) or contaminated (845/16899; 5%). A comparison of the total number of patients who were referred for diagnosis and treatment (954/666 patients, P > 0.05) showed a 30.1% reduction during the COVID-19 pandemic. Although, with these low number of patients, the significant increases of NTM species (P < 0.05) among suspected TB pulmonary patients were observed. Besides, new species of NTM, for example, Mycobacterium peregrinum and Mycobacterium montefiorense, were detected. For the past 20 years, these two species were not reported from pulmonary patients in Iran. Conclusions: During the pandemic of COVID-19, the TB diagnosis network became irregular, as a consequence, many patients could not reach the treatment center, and this could increase the circulation of mycobacterial diseases (TB and NTM). The study shows the emergence of new opportunistic NTM species also.

Keywords: COVID-19, Mycobacterium montefiorense, Mycobacterium peregrinum, nontuberculosis Mycobacteria

How to cite this article:
Aghajani J, Farnia P, Farnia P, Ghanavi J, Saif S, Marjani M, Tabarsi P, Moniri A, Abtahian Z, Hoffner S, Velayati AA. Effect of COVID-19 pandemic on incidence of mycobacterial diseases among suspected tuberculosis pulmonary patients in Tehran, Iran. Int J Mycobacteriol 2022;11:415-22

How to cite this URL:
Aghajani J, Farnia P, Farnia P, Ghanavi J, Saif S, Marjani M, Tabarsi P, Moniri A, Abtahian Z, Hoffner S, Velayati AA. Effect of COVID-19 pandemic on incidence of mycobacterial diseases among suspected tuberculosis pulmonary patients in Tehran, Iran. Int J Mycobacteriol [serial online] 2022 [cited 2023 Feb 5];11:415-22. Available from: https://www.ijmyco.org/text.asp?2022/11/4/415/363163

  Introduction Top

Medical coverage and success rates are ongoing challenges for low- and middle-income countries.[1],[2],[3],[4],[5] Due to the coronavirus SARS-CoV-2 pandemic (2019), many health, social, and economic services were affected.[6],[7],[8],[9],[10],[11] In many countries, resources for controlling tuberculosis (TB) were reallocated to meet increasing threats caused by the corona pandemic. During the past 2 years of the pandemic, TB control has suffered from limitations in hospital beds and laboratory facilities, and additionally, due to COVID-19 travel restrictions, many patients could not get their medical treatment on time.[12],[13],[14] The condition was effected almost all the TB endemic countries, so for the first time in 10 years, the World Health Organization (WHO) reports increasing TB incidence and death globally.[15] The corona pandemic has thus caused widespread disruption to the health system through limiting routine health services, low access to medical care, and reduced diagnosis, not only for TB but also for other infectious diseases.[16],[17],[18],[19],[20],[21],[22] For example, analysis of TB impact modeling studies showed delayed diagnosis and TB-related deaths up to 20%, which can be even more in coming years.[6],[23] WHO reported that global TB mortality has risen from 1.4 million to 1.5 million, not because of a direct resurgence of TB, but because of the COVID-19 pandemic, which has put severe pressure on the health-care system in most of the countries.[24] Indeed, the COVID-19 pandemic has seriously affected the activities of the Zero TB project.[9],[24] Thereby, it is an alarming situation for TB and nontuberculous mycobacteria (NTM) services. It has already been reported that TB notification during the second quarter of 2020 decreased by 35.5% compared to the second quarter of 2019, which is six times more than the average annual decrease of 5.1% recorded during 2015–2019 in the European Region.[25],[26] Unfortunately, as no proper information is available on the impact of the COVID-19 pandemic on mycobacterial laboratories, the pronounced increase of mycobacterial diseases should not be ignored.[9],[27],[28] In the year 2015, Velayati et al. reviewed circulating NTM strains (clinical and environmental samples) that were reported in the past 22 years in Iran.[29] A total of 997 NTMs were found whereof the rapidly growing mycobacterial (RGM) species Mycobacterium fortuitum (229/997; 23%) was most commonly isolated in both clinical (28%) and environmental (19%) samples. Among slow-growing mycobacteria (SGM), Mycobacterium simiae (103/494; 21%) was more common in clinical samples while in environmental samples was Mycobacterium flavescens (44/503; 9%).[29]

NTM-related infections have been reported in different geographical places.[26],[27],[30],[31] Mycobacterium abscesses and their subspecies often affecting children and Mycobacterium avium complex members usually affect adults suffering from human immunodeficiency virus.[32] The lung is a common site of human mycobacteriosis. Manifestations range from asymptomatic to cavitary disease, and X-rays may show fibrosis, upper lobe cavity, nodular or parenchymal opacity, and thickening of the pleura.[33] The elderly populations are mostly affected cases because of predisposed lung conditions (such as silicosis, obstructive pulmonary disease, pneumoconiosis, previous TB, bronchiectasis, or cancer).[33],[34]. In the present study, we aimed to investigate and compare the impact of the COVID-19 pandemic on TB services in Iran. For these reasons, we first analyzed the number of suspected TB pulmonary cases who were referred to the National Reference TB Laboratory (NRL TB) before the COVID-19 pandemic (January 2018–December 2019) and during the COVID-19 pandemic (January 2020–December 2021). The isolated NTM species were analyzed, and the emergence of the new opportunistic species of NTM was reported. The study showed not only the TB infrastructure was affected, but also the COVID-19 pandemic causes increase in NTM diseases.

  Methods Top

Sample collection

In this study, the clinical specimens, including sputum, bronchial lavage, pleural effusion, and transbronchial lung biopsy, were collected from patients referred from other TB laboratories in Iran or patients who were hospitalized to the National Research Institute of Tuberculosis and Lung Disease (NRITLD), Tehran, Iran, between January 2018 and December 2021. A total of 7401 patients with suspected TB infection (clinical specimens = 16,899) were examined from January 2018 to December 2021, of which 3888 (23%) clinical specimens were acid-fast bacillus (AFB) culture positive for mycobacteria that belong to 1620 patients. A majority of 88.1% (3457) was M. tuberculosis and 431 cases (11.9%) were isolated as NTM [Table 1]. The remaining cultures were either negative (12156/16899; 71.9%) or contaminated (845/16899; 5%). This study was approved by the Scientific Ethical Committee of NRITLD, Shahid Beheshti University of Medical Sciences, Tehran, Iran (IR.SBMU.NRITLD.REC.1400.020). All the patients agreed to participate in the study and filled out the consent forms.
Table 1: Positive isolation rate of mycobacteria between the study period 2018-2021

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Mycobacterium isolation and identification

Primary isolation of mycobacterial strains was done on Löwenstein–Jensen medium.[35] Then, DNA from the isolated mycobacteria was extracted using the Qiagen kits[36] and estimated by gel electrophoresis. To identify Mycobacterium species, as a first step, the GeneXpert system was used to separate the TB from NTM species, and then, all isolates of NTMs were identified by three genes, IS6110, Hsp65, and 16s-23s rRNA, based on Telenti et al.[37] and Brunello et al.[38] methods. For the IS6110, Hsp65, and 16s-23s rRNA genes, the primers Tb1 and Tb2 - Tb 15, Tb17, Tb11, Tb12 - and SP1, SP2 were used respectively [Table 2]. IS6110 gene gives a 190 bp fragment that was visualized by 1.2% agarose gel electrophoresis. The polymerase chain reaction (PCR) product of Hsp65 was 439 bp that was digested by the restriction enzymes BstE II and Hae III and thereafter observed using 8% acrylamide gel electrophoresis. The obtained patterns were analyzed using PARASITE websites (www.app.chuv.ch/prasit). The PCR products of 16s-23s rRNA were from 220 to 350 bp, which were accordingly digested using different restriction enzymes HaeIII, CfoI, TagI, MspI, DdelI AvaII, and HinfI (mainly based on obtained fragments). The frequency of isolates was calculated using SPSS version 23 (IBM SPSS, Armonk, NY, USA) and Microsoft Excel software (version 2016, Microsoft Corporation, Redmond, WA, USA).
Table 2: Primers used in the study

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  Results Top

Patients were divided into two groups: “Group A” that consisted of 11,679 specimens from 4866 suspected TB pulmonary cases from 2018 to 2019 (before COVID-19) and Group B that had 5220 specimens from 2175 patients from January 2020 to December 2021 (during the ongoing COVID-19 pandemic). In Group A, mycobacteria were isolated by culture in 19.6%, 2290 out of the 11,679 samples, derived from 954 cases with pulmonary infection, of these cases, 852 patients 89.3% (2046/2290) had M. tuberculosis and the remaining 102 patients (246 isolates 10.6%) was NTM [Table 1]. The rate of NTM isolates for slow-growing mycobacteria (SGM) was 73.7% (180/244; 71 patients) and for RGMs was 26.0% (64/224; 31 patients). As shown in [Table 3] and [Figure 1], the higher SGM belongs to pulmonary patients; 47 patients were infected with M. simiae (127/180 specimens [70.6%]) and 13 patients had Mycobacterium intracellular (35/180 specimens [19.4%]). Among the more frequent species in RGM, most patients had Mycobacterium abscessus 60/64 (93.75%; 29 patients) and two Mycobacterium chelonae 3/64 (4.7%; 2 patients) [Table 3] and [Figure 1].
Table 3: The number and type of nontuberculous mycobacteria during the study period 2018-2021

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Figure 1: Distribution of NTM species isolated from clinical sample during the study period 2018–2021. (a) NTM isolation before COVID-19. (b) NTM isolation after COVID-19. NTM: Nontuberculous mycobacteria

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In Group B, mycobacteria were isolated by AFB-positive culture in 30.6%, 1596 out of 5220 samples, derived from 666 cases with pulmonary infection, of these cases, 588 patients 88% (1411/1598) had M. tuberculosis and the remaining 78 patients (187 isolates 11%) was NTM [Table 1]. The rate of NTM isolates for SGM was 75.4% (141/187; 56 patients) and for RGMs was 24.6% (46/187; 22 patients). As shown in [Table 3] and [Figure 1], the higher SGM belongs to pulmonary patients; 28 patients were infected with M. simiae (85/187 specimens [45.4%]) and 14 patients had M. intracellular (29/187 specimens [15.5%]). Among the more frequent species in RGM were M. abscessus 38/187 (20.3%; 14 patients) and M. chelonae 3/187 (1%; 2 patients)

In total, a comparison of AFB-positive pulmonary patients in the two groups showed a 30.1% reduction (n = 954/666 patients) during the COVID-19 pandemic [Table 1] and [Table 3] and [Figure 2]. The results also showed that out of 954 cases/102 patients (10.6%) and out of 666 cases during the COVID-19 pandemic, 78 patients (11%) had NTM infection. Although, statistically not significant, but comparing the number of AFB-positive cases (n = 954/666) showed two-fold increases of NTM isolates (n = 102/78).
Figure 2: Number of samples and positive rate for mycobacteria during the 4-year study period

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Besides, it is important to mention that the two new opportunistic NTM species, i.e. Mycobacterium peregrinum and Mycobacterium montefiorense, from pulmonary samples were also detected [Figure 3] and [Figure 4]. These isolates have been detected for the first time in the pulmonary samples in the past 20 years in Iran. The M. montefiorense strains samples were sent from the south of Iran (Ahvaz, which is near the Persian Gulf) and the other one (M. peregrinum) send from Tehran University. Unfortunately, we have no information about their treatment and disease progress. The geographical distribution of NTM showed a new appearance of RGM and SGM in five (Golestan, Mazandaran, Hamedan, Kohgiluyeh and Boyer-Ahmad, and Qom) and two (Gilan and Chaharmahal and Bakhtiari) provinces of Iran, respectively.
Figure 3: Identification of Mycobacterium peregrinum. (a) Digestion of 16s-23s rRNA product with HaeIII and CfoI restriction enzymes. (b) Digestion of Hsp65 product with BsteII and HaeIII restriction enzymes

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Figure 4: Identification of Mycobacterium montefiorense. (a) Digestion of 16s-23s rRNA product with HaeIII and CfoI restriction enzymes. (b) Digestion of Hsp65 product with BsteII and HaeIII restriction enzymes

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  Discussion Top

The negative impact of the COVID-19 pandemic on the detection and control of TB is well documented worldwide.[16],[39],[40],[41],[42],[43],[44] In this study, we showed a 31% reduction in the number of samples received in NRL TB. The reduction in sample size may be due to the imposed travel restriction and/or temporary provisional laboratory closure within the country. Even TB pulmonary patients were afraid of coming to the hospital where the COVID-19 diagnosis was going on. Some of the patients and doctors were more intellectual to keep their contact by the online system. Although, in overall, the well-established networks were damaged. The present results showed that from 954 TB patients, isolates from only 666 of them were sent to our TB reference laboratory during the COVID-19 pandemic (69.8%); whereas when we analyzed the receiving samples, the reduction was even higher (11679/5220; 44.6%). This means the patients had not given second or third samples as per standard protocols [Table 1]. In the same way, the regional laboratories that sending their sample for subtyping of NTM to the referral center was affected. As such, most of the mycobacteriology laboratories have infrastructure to detect TB from NTM, and this is NRL TB duties to identify NTM subspecies. Thereby, NRL TB has always a regular system to check the NTM ratio and species variation using geographical information systems.[45],[46] At NRL TB, the samples first identify using a GeneXpert device, then to identify TB from NTM, we proceed with routine PCR, PCR-restriction fragment length polymorphism, and nested PCR using IS6110, Hsp65, and 16s-23s rRNA methods [Table 2].

Pulmonary diseases caused by NTM infections is neglected for years in many resource-limited countries, most of the control strategies have been focused on the detection and control of active TB and to some extent also latent TB cases.[47] Therapeutic drugs and susceptibility tests are mainly for TB, and much less is known about NTM drug resistance and optimally treat patients infected with them.[48],[49],[50] We already showed the distribution of NTM in Iran based on 22 years of published data from all over the country. In the same report, we highlighted that only 9–10 laboratories out of 465 governmental TB laboratories were capable of distinguishing TB from NTM.[29] Furthermore, the identification methods in those laboratories were typically based on classical phenotypic methods,[51] which might increase the risk of contamination, and they could just identify species and not their subspecies. Whereas, in NRL TB and other well-established institutes like the Pasteur institute of Iran, the identification using molecular level reaches to subspecies and/or subtypes of NTM.

During the 2 years of the COVID-19 pandemic, due to lockdown systems and previously used medical treatment protocols (remdesivir 200 mg on the first day 1, and 100 mg plus dexamethasone 8 mg for 5 days), we were very much concerned about raises in opportunistic species of NTMs and activation of latent TB. As shown in [Table 1] and [Table 3] and [Figure 2], the incidence of NTM species from pulmonary samples was increased. By epidemiological investigation, we could not estimate properly how many cases had coinfection with COVID-19, but as the hospital became a COVID-19 referral center during the pandemic, most of the samples (±60%–80%) that were received in the years 2020–2021 had either COVID-19 or were post-COVID-19 cases.[52],[53],[54],[55] The coinfection of M. simiae and COVID-19 among pulmonary patients was detected. The findings raise the question that if an increase in NTM infection could be related to post-COVID-19 diseases or not? The question needs further studies among COVID-19 cases. It has been already known that the increases in NTM pulmonary infection occur during receiving immunosuppression therapy, i.e. dexamethasone. Few studies outline the elderly population with a high incidence of NTM.[34],[56],[57] Similarly, Iran is among the countries which are moving toward an aging population. It is well known that older people suffer from weakened immune systems and are more susceptible to developing various underlying diseases, which might greatly increase the risk of NTM infection in them.

The results showed [Figure 3] and [Figure 4] a new opportunistic NTM species from pulmonary patients that had not been reported in Iran before. M. peregrinum and M. montefiorense were the two species of NTMs that we isolated for the first time from pulmonary patients. M. peregrinum is a member of the RGM, a subspecies of the fortuitum group. These organisms are ubiquitous and are found in soil and water.[58],[59] They may occasionally be found as common organisms on human skin.[60] Causes infections of the skin, surgical sites, and center lines.[58] Most documented human infections include anterior thoracic infections such as tunnel catheter infections, sternotomy wound infections, and infections after augmentation mammoplasty.[61],[62] In addition, M. peregrinum is involved as a possible cause of lung disease in humans.[63],[64] What we know about this patient is that he was just referred to the hospital with pulmonary symptoms. No other information, we could collect from the patient. As the sample was isolated from pulmonary patients and the optimal treatment for M. peregrinum infection has not yet been developed, we are deeply concerned about its prevalence within the country.

M. montefiorense is SGM that was first described in 2003 based on strains isolated from moray eels.[65] 16S rRNA sequence analysis shows that M. montefiorense is most closely related to M. triplex, an opportunistic human pathogen.[65] Information about this species is very limited, but so far, it has been isolated from environmental sources such as water, sludge, fish tanks, and animal tissues.[66] Its clinical relevance to humans is not yet known. We suggest that there should be an urgent mechanism for monitoring and scrutinizing NTMs within the country. Samples of this patient are reserved in the Gene-bank of NRL TB for further study. Based on geographical information system distribution, our result showed a new appearance of RGM and SGM in five (Golestan, Mazandaran, Hamedan, Kohgiluyeh and Boyer-Ahmad, and Qom) and two (Gilan and Chaharmahal and Bakhtiari) provinces of Iran, respectively. We had no pulmonary infection reports from these regions before the COVID-19 pandemic. The pulmonary sample collection in larger number is going on to understand the reasons behind these changes within these provinces of Iran.

  Conclusions Top

As long as the whole focus of society is on the COVID-19 pandemic, we had missed the raises of other infectious diseases like opportunistic NTM infections. If the health-care systems continue to ignore the NTM, a new clinical challenge with significant morbidity and mortality is expected. Our results emphasize the potential importance of NTMs and its frequency across the country. Finally, the results of the present study underline the need to establish more specialized centers for NTM detection. In addition, comprehensive research is essential to increase our understanding of how to best detect, treat, and control opportunistic NTM infections. Because NRL TB is a reference center for TB and NTM in the country, the data we presented in this study are related to samples of patients coming from various provinces of Iran and/or positive culture that send to the center for identification and susceptibility testing. In many cases, we could not perform the follow-up of patients and due to incomplete baseline information like NTM coinfection with COVID-19, results relate to COVID-19 and NTM infection, could not be presented for all patients.

Limitation of study

There was limitation in transporting the specimens during the COVID-19 within TB laboratory net works.

Ethical clearance

The study was approved by the institutional Ethics Committee of NRITLD, Shahid Beheshti University of Medical Sciences, Tehran, Iran (IR.SBMU.NRITLD.REC.1400.020).

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2], [Table 3]


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