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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 2  |  Issue : 3  |  Page : 184-190

Mycobacterium farcinogenes and Mycobacterium senegalense as new environmental threats


1 Mycobacteriology Research Center (MRC), National Research Institute of Tuberculosis and Lung Disease (NRITLD), Tehran, Iran
2 Department of Biotechnology, School of Advanced Technology in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Date of Web Publication6-Sep-2018

Correspondence Address:
Dr. Jafar Aghajani
Mycobacteriology Research Center, National Research Institute of Tuberculosis and Lung Disease, Shahid Beheshti University of Medical Sciences, Tehran
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/bbrj.bbrj_67_18

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  Abstract 


Background: Mycobacterium farcinogenes and Mycobacterium senegalense are the causes of the bovine farcy, a chronic granulomatous disease of the skin of zebu cattle. The zoonotic potential of these bacteria is unclear. The high contamination rate of these bacteria (as species of nontuberculous mycobacteria) has been reported in environmental samples. This study aimed to determine the prevalence of these bacteria in the water and soil environment in four suburbs of Tehran, Iran. Methods: A total of 4014 soil and water samples were collected from four areas of Tehran including Robat Karim, Firuzkuh, Shahr-e-Ray, and Varamin. In each city, at least one sample was collected per 1002 m. The sediment samples were cultured on the Lowenstein–Jensen medium. Twice a week was observed to study the growth of colony, morphology, and pigmentation. Colonies were studied using phenotypic tests. Molecular analysis was also carried out on colonies. Results: Among samples, the number of collected water samples was 48.48% (1946/4014), and the number of soil samples was 51.51% (2068/4014). Results of cultures from collected samples showed that 21.47% (862/4014) of them were positive. Among the studied areas, Rabat Karim has been identified as the most polluted region (169/480; 35%). The abundance of M. farcinogenes has been dominant in Ray. The least infection has been reported in Varamin. Conclusion: The results showed that the prevalence of these two strains was very high in water and soil. Due to these two strains are the main and effective factors of bovine farcy in zebu cattle (the most farmed cows in Iran), surveillance of the zoning potential of this disease is very important.

Keywords: Mycobacterium farcinogenes, Mycobacterium senegalense, nontuberculous mycobacteria, water and soil pollution


How to cite this article:
Aghajani J, Rajaei E, Farnia P, Malekshahian D, Seif S. Mycobacterium farcinogenes and Mycobacterium senegalense as new environmental threats. Biomed Biotechnol Res J 2018;2:184-90

How to cite this URL:
Aghajani J, Rajaei E, Farnia P, Malekshahian D, Seif S. Mycobacterium farcinogenes and Mycobacterium senegalense as new environmental threats. Biomed Biotechnol Res J [serial online] 2018 [cited 2021 Dec 8];2:184-90. Available from: https://www.bmbtrj.org/text.asp?2018/2/3/184/240705




  Introduction Top


Mycobacterium farcinogenes and Mycobacterium senegalense are the cause of the bovine farcy, a chronic granulomatous inflammation and progressive disease of the skin and lymphatics of zebu cattle (zebu cattle are cows with long horns that are the most farmed cows in Iran).[1],[2],[3] Edmond Nocard described the first causal agent in 1888; the lesions were sent to him by M. C. Couzin (a veterinarian at Marie-Galante in Guadeloupe). The agents were Gram-positive, acid-fast, and aerobic actinomycetes.[4],[5] According to a discovery by Nocard, the disease was associated with Nocardia species, and Nocardia farcinica was recognized as the causal agent.[6],[7],[8]

At first, it seemed that the disease is caused by N. farcinica; however, now, it is clear M. farcinogenes and M. senegaleme are the principal agents.[9] Chemical and serology analysis revealed that N. farcinica can be clearly distinguished from both M. farcinogenes and M. senegalense.[10],[11]

In 1973, Chamoiseau introduced and recognized these two species.[12] The molecular analysis confirmed that M. farsinogen and M. sengalens are in a subclade together with Mycobacterium houstonense and Mycobacterium fortuitum. This subclade is close to one accommodating Mycobacterium peregrinum, Mycobacterium porcinum, Mycobacterium septicum, Mycobacterium neworleansense, and Mycobacterium alvei.[1]

Based on the phenotypic differences, Chamoiseau [12] presented these two species, which have first appeared in the 1st edition of the manual of Bergey's Manual of Systematic Bacteriology.[13]

It is demonstrated that M. farcinogenes and M. senegalense can be also distinguished based on the histopathological behavior,[12] DNA dependence, Mycobacterium content,[14] chemotaxonomic and biochemical properties,[15],[16],[17] pyrolysis mass spectrometry,[18] and 16S rRNA sequencing data.[15],[19],[20],[21],[22],[23]

M. farcinogenes and M. senegalense strains contain mycolic acids, 2-alkyl 3-hydroxy long-chain fatty acids, that can be separated into α', α, and epoxymycolates. The same mycolic acid template has been identified in Mycobacterium chitae, M. fortuitum, M. peregrinum, and Mycobacterium smegmatis strains.[11],[19],[20]

According to the previous studies, the analysis of the sequence of 16srna suggests that the species M. farsinogen and M. sengalens relate to each other and to rapidly growing nonchromogenic mycobacteria.[4],[21] DNA probes for M. farcinogenes (5'-ACTACAGATGCTGGCTGA) and M. senegalense (5'-CACTACAGCGCACAGACTCCTCAC) have been designed and are available for 16S–23S rDNA spacer sequences.[22]

Lowenstein–Jensen (L. J) is a medium that is commonly used to selectively isolation of M. farsinogen from many other mycobacteria from infected materials.[23],[24] After 2–5 days (M. senegalense) and 5–10 days (M. farcinogenes) at 25°C–37°C in the L. J medium, the harsh, complex, and twisted colonies that are fully connected to the media are evident.[4] Modified Sauton's broth [25] is generally used for the cultivation of biomass from M. farsinogen, M. sanguinase, and some mycobacteria for chemotaxonomic studies.[11],[16],[26],[27],[28]

The M. farcinogenes can be microscopically shown on a direct smear of clinical samples and on prepared tissue materials. This appearance is distinct and sufficient for the initial diagnosis of bovine farcy and its distinction with tuberculosis (TB).[5],[7],[8],[27],[29],[30],[31],[32],[33],[34],[35] Several documentations are available regarding the prevalence, frequency, and also the zoonotic potential of these bacteria. Bovine farcy has been reported from 19 countries that are located in Africa, Asia, Latin America, and the Caribbean and have tropical and subtropical climatic.[8],[27],[36] Historically, it extends into the East (including South India, Sri Lanka, and Sumatra) and the West (including the north of Latin America and West Indies, but predominantly in sub-Saharan Africa).[4],[8],[30],[37],[38],[39],[40],[41],[42],[43],[44]

The potential of zoonotic M. senegalense and M. farcinogenes is uncertain. Only a small number of reports provide evidence that M. senegalens[45] and M. farcinogenes[46] cause an infection in human.

Booth et al.[5] reported the first case of atypical Mycobacterium infection after total knee arthroplasty in 1979. The patient was infected with M. fortuitum.[46] Wong et al.[46] reported the first infection of M. farsinogen in a 67-year-old female with a history of traumatic fracture of the left femur. The patient and surgeons did not have any history of contact with the animal.[46]

In 2005, Oh et al. described a case of blood infection with M. senegalens in South Korea.[47] Surveying the mentioned bacteria in patients revealed their zoonotic nature and indicated that the spread of Mycobacterium species associates with the human infection. However, these species are also evaluated in environmental samples.

Rapidly growing mycobacteria (RGM) such as the M. fortuitum are capable to grow in a very hostile environment.[48] Resistant RGM species are commonly found in municipal tap water.[49],[50] A study by Carson et al.[49] showed that 55% of hemodialysis centers for the city's water intake in the United States included RGM. Recently, the acid-fast mycobacteria were detected in more than 90% of biofilms (slime layer present at water and soil interfaces) taken from piping water systems.[51] In 2014, Velayati et al. examined the molecular epidemiology of nontuberculous mycobacteria (NTM) in clinical and environmental samples. In their study, interestingly, 7%–10% of samples of water and 15%–6% of soil samples collected from the suburb of Tehran were inhabited by NTM. Furthermore, they reported a case of M. farcinogen infection.[52] In another study, Azadi et al. examined mycobacteria in the hospital environment and showed the potential pathogenesis of these opportunistic bacteria.[53] The existence of these evidence indicates that investigation of the frequency and prevalence of these species in environmental samples is of importance. These species should be considered as pathogenic agents in humans due to their potential for pathogenicity and their zoonoticity.

We also intend to investigate the frequency and prevalence of M. farcinogen and M. senegalense in environmental samples.


  Methods Top


In total, 4014 soil and water samples were collected from four regions of Tehran including Robat Karim (27 km Southwest of Tehran downtown), Firuzkuh (147 km Northeast of Tehran downtown), Shahr-e-Ray (14 km Southeast of Tehran downtown), and Varamin (35 km Southeast of Tehran downtown). In each area, at least one sample was collected per 100 square meters.[52]

Approximately 6 g of soil was collected from a depth of 3–5 cm and suspended in a sterile tube of 50 ml, and then, the process was performed in a manner previously described by Portaels et al.[12] Briefly, 0.5 g of the soil (wet weight) was suspended in malachite green 0.2% (5 ml) and cycloheximide (1 ml at 500 mg/ml). After abrupt shaking, 1 mol of NaOH was added and stored at room temperature for 30 min. The mixture was centrifuged for 15 min at 2000 g, and oxalic acid (10 ml of 5%W/V) was added to the sediment.[52] The centrifuge was repeated for 15 min, and the sediments were cultured on L. J culture medium.[52]

For water samples, 50–100 ml of diversifying water resources (running water, Tap water, Water remains) was collected. The collected water samples were first decontaminated with cetylpyridinium chloride (final concentration of 0.05%) for 30 min and then digested using standard protocol.[54] Sediments of each treated specimen were used to prepare a Ziehl–Neelsen smear and cultured in a L. J medium.[54] For culture, sediments (200 ml of sediments/per tubes) were inoculated into three L. J medium and incubated at 37°C, 25°C, and 42°C for 12 weeks.[54]

Inoculated cultures were observed twice a week to studied growth rate, colony, and pigmentation morphology. Colonies were examined for acid fastness and phenotypic testing (niacin, nitrate, catalyze, iron uptake, and arylsulfatase activity). Molecular analysis was performed on single cell culture from isolation culture.[55]

Water and soil samples

A total of 4014 soil and water samples were collected from four areas of Tehran. The number of collected water samples was 48.48% (1946/4014), and the number of soil samples was 51.51% (2068/4014). The results of the positive cultures from the collected samples showed that 21.47% (862/4014) of them were positive.

In general, M. farcinogenes (126/4014; 3.13%) and M. senegalense (52/4014; 1.29%) had a high frequency in soil and water samples [Table 1]. Among the studied regions, Robat Karim was identified as the most contaminated (169/480; 35%) area although the frequency of M. farcinogenes was more dominant in Shahre-Ray. The lowest contaminated region was Varamin. Other isolated non-tuberculosis mycobacterium that were not considered in this study include Mycobacterium kansasii 54 (6.26%), Mycobacterium simiae 46 (5.33%), Mycobacterium gordonae 42 (4.87%), M. fortuitum 72 (8.35%), Mycobacterium parafortuitum 44 (5.10%), Mycobacterium chelonae 24 (2.7%), and Mycobacterium conceptionense 20 (2.3%) [Table 1].
Table 1: Frequency of positive samples among different water and soil samples in different regions

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Comparison of HaeIII and BstEII RFLP patterns from isolates of M. senegalense and M. farcinogenes isolates from soil and water is shown in [Figure 1]. The digested pattern of the PCR product by SP primer was different in the mentioned species. Digested pattern for M. farcinogenes was 190–110 bp and 168–132 bp. The pattern for M. senegalense was 148–109 bp and 174–72 bp. The digested pattern of PCR product by HSP primer produced single pattern, i.e., 234-120-80 bp with restriction enzyme BsteIII and 140-125-60-55 bp with restriction enzyme HaeIII [Figure 1].
Figure 1: Comparison of HaeIII and BstEII RFLP patterns from isolates of Mycobacterium senegalense Type 1 (a), Mycobacterium senegalense Type 2 (b), and Mycobacterium farcinogenes (c) isolates from soil and water

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Of the water samples collected (1946/4014; 48.48%), the number of positive samples was 27.69% (539/1946). The collected water samples were from running water (1396/1946, 71.73%), tap water (290/1946, 14.90%), and water remains (260/1946; 13.36%). The result showed that the 19.65% (79/539) of the samples was related to M. farcinogenes. About 5% of samples belonged to M. senegalense (Type 1 (14/539; 3.52%) and M. senegalense Type 2 (8/539; 1.48%). It should be noted that the most positive water samples were M. farcinogenes (41/1946; 2.10%) in Shahre-Ray. Running water was more contaminated than other studied water samples [Table 2].
Table 2: The sources of water samples collected from different locations

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Out of soil samples collected (2068/4014; 51.51%), the number of positive samples was 51.61% (323/2068). Among the studied region, Robat Karim was identified as the most comminuted (64/231; 27.7%) area, and the frequency of M. farcinogens dominated in this region. The lowest comminuted region was Varamin [Table 3].
Table 3: Isolated samples from soils of the studied regions

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Geographic information system analysis

The prevalence of mycobacteria was recorded and analyzed in different regions with geographic information system (GIS) software. In this regard, GIS plays an effective role in data collection and analysis with robust analytical performance.[56],[57] Therefore, GIS evaluates the prevalence of different geographical areas by collecting information and managing epidemiological data and describing the severity of the disease.[56],[57] [Figure 2] shows the geographic and spatial distribution of different isolates. [Figure 2] shows that in water samples, M. farcinogenes, and M. senegalense Type 1 are the most frequent in Shahre-Ray, and M. senegalense Type 2 has the highest frequency in the Varamin. It was also found that in soil samples, M. farcinogenes and M. senegalense Type 1 had the highest percentage of prevalence in Shahre-Ray and M. senegalense Type 2 had the least percentage of prevalence in this city. According to the results presented in [Figure 2], it can be said that M. farcinogenes is significantly expanding in soil and water samples. It was also revealed that M. farcinogenes had the highest prevalence in Shahre-Ray and in soil samples had the highest percentage of prevalence in Robat Karim. Shahre-Ray had the highest prevalence among other areas [Figure 2].
Figure 2: Geographic distribution and frequency of the mycobacterial species in the samples collected from the suburbs of Tehran

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  Discussion Top


The aim of the present study was an examination of the prevalence of M. farcinogenes and M. senegalense as the main cause of bovine farcy disease of the skin and lymphatics of zebu cattle in soil and water samples of some different areas.

Bovine farcy has become a new global concern. Due to its economic impact on animal production, the potential spread of wildlife pollution and the risk of transmitting the disease to humans.

Due to the comprehensive ability of rapidly and slow-growing mycobacteria, there is an increasing incidence of human infection with these mycobacteria around the world.[58],[59] Particularly, rapidly growing mycobacteria are known as one of the most important pathogens in hospital infections, such as catheter infections in immunocompromised hosts, as well as in implants infections. Among the rapidly growing mycobacteria, the M. fortitum is the most commonly mycobacterial pathogen in the clinical situation.[48],[60],[61]

Due to the difference in sensitivity among species, rapid identification, and sensitivity testing are necessary to select the appropriate antibiotic agent against the desired Mycobacterium.[62] Due to the resistance of atypical mycobacteria to traditional TB drugs, use of public antibiotics is very challenging. Each item should be cultivated separately, and the type of germs must be identified. In these cases, collaboration with a microbiologist is required.

There are many reports that have been published about the prevalence and infections of M. farcinogen and M. Senegalens in humans.[47],[48],[63],[64],[65] In all clinical reports, it is important that patients have no connection with animals, livestock, and patients who are infected with these bacteria.[47]

This fact highlights the role of the environment and in particular, the importance of environmental samples. According to the documentation for the high prevalence of this species in samples of water, soil, and hospital environments, the importance of this issue is clear.[4],[66]

The results of this study showed that the prevalence of two mentioned strains was high in both soil and water. Since these two strains are the main and influential factor of bovine farcy disease in zebu cattle (the most farmed cows in Iran), the monitoring of zoonotic potential of this disease is very important.

Positive bacteria in the water sample rate equal to 27.69% and 15.61% related to the positive samples in the soil, this indicates the high prevalence of these bacteria in environmental samples.

Interestingly, M. farcinogenes was the most common isolated strain from the environment, especially in water samples. The high prevalence of these bacteria in water samples is alarming. The data obtained in our study revealed that slow-growing mycobacteria such as M. farcinogenes are the predominant isolated NTM from soil and water. Due to the high prevalence of M. farcinogenes in the suburbs of Tehran and its potential pathogenesis for livestock and humans, more epidemiological studies are needed.

With the advancement of molecular techniques, it is possible to identify and cultivate the samples of these bacteria. Since these bacteria produce symptoms such as TB, correct and early diagnosis is needed to choose a more effective treatment strategy.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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