• Users Online: 405
  • Print this page
  • Email this page

 Table of Contents  
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
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/bbrj.bbrj_67_18

Rights and Permissions

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 2022 Jan 23];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

Click here to view

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

Click here to view

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

Click here to view

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

Click here to view

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

Click here to view

  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


Conflicts of interest

There are no conflicts of interest.

  References Top

Hamid ME. Current perspectives on Mycobacterium farcinogenes and Mycobacterium senegalense, the causal agents of bovine farcy. Vet Med Int 2014;2014:247906.  Back to cited text no. 1
Chamoiseau G. About the etiology of streptothricosis of the Chad zebu cattle: Nocardiosis or mycobacteriosis ? III. Amidasic activity. Journal of tropical livestock science1972;25:191-4.  Back to cited text no. 2
Chamoiseau G. The etiology of Chadian zebu farcin: Nocardiosis or mycobacteriosis? I. Bacteriological and biochemical study. Journal of tropical livestock science1969;22:195-204.  Back to cited text no. 3
Hamid ME. Epidemiology, pathology, immunology and diagnosis of bovine farcy: A review. Prev Vet Med 2012;105:1-9.  Back to cited text no. 4
Nocard E. Note on the disease of cattle of Guadeloupe known as the farcy. Ann Inst Pasteur 1888;2:293-302.  Back to cited text no. 5
Trevisan VB. The genera and species in batteriacee. L. Zanaboni and Gabuzzi. Milan; 1889.  Back to cited text no. 6
Nocard E, Leclainche E. Microbial diseases of animals. Masson and Cie;1903.  Back to cited text no. 7
Mostafa I. Bovine nocardiosis (Cattle farcy). A review. Vet Bull Weybridge 1966;36:189-93.  Back to cited text no. 8
Chamoiseau G. Etiology of farcy in African bovines: Nomenclature of the causal organisms Mycobacterium farcinogenes. International Journal of Systematic and Evolutionary Microbiology 1979;29:407-10.  Back to cited text no. 9
Ridell M. Immunodiffusion Studies of Mycobacterium, Nocardia, and Rhodococcus for Taxonomic Purpose. Vol. 11. Stuttgart, Germany: Actinomycetes Gustav Fisher Verlag; 1981. p. 235-41.  Back to cited text no. 10
Ridell M, Goodfellow M, Minnikin DE, Minnikin SM, Hutchinson IG. Classification of Mycobacterium farcinogenes and Mycobacterium senegalense by immunodiffusion and thin-layer chromatography of long-chain components. J Gen Microbiol 1982;128:1299-307.  Back to cited text no. 11
Portaels F, De Muynck A, Sylla MP. Selective isolation of mycobacteria from soil: A statistical analysis approach. J Gen Microbiol 1988;134:849-55.  Back to cited text no. 12
Wayne LG. “Genus Mycobacterium lehmann and neumann 1896 363 ALM. In: Sneath PH, Mair NS, Sharpe ME, Holt JG, editors. Bergey's Manual of Systematic Bacteriology. Md, USA: Williams & Wilkins Baltimore; 1986.  Back to cited text no. 13
Hall RM, Ratledge C. Equivalence of mycobactins from Mycobacterium senegalense, Mycobacterium farcinogenes and Mycobacterium fortuitum. J Gen Microbiol 1985;131:1691-6.  Back to cited text no. 14
Ridell M, Goodfellow M. Numerical classification of Mycobacterium farcinogenes, Mycobacterium senegalense and related Taxa. J Gen Microbiol 1983;129:599-611.  Back to cited text no. 15
Hamid ME, Minnikin DE, Goodfellow M. A simple chemical test to distinguish mycobacteria from other mycolic-acid-containing actinomycetes. J Gen Microbiol 1993;139:2203-13.  Back to cited text no. 16
Hamid ME, Chun J, Magee JG, Minnikin DE, Goodfellow M. Rapid characterisation and identification of mycobacteria using fluorogenic enzyme tests. Zentralbl Bakteriol 1994;280:476-87.  Back to cited text no. 17
Magee JG, Goodfellow M, Sisson PR, Freeman R, Lightfoot NF. Differentiation of Mycobacterium senegalense from related non-chromogenic mycobacteria using pyrolysis mass spectrometry. Zentralbl Bakteriol 1997;285:278-84.  Back to cited text no. 18
Dobson G, Minnikin D, Minnikin S, Parlett J, Goodfellow M, Ridell M, et al. Systematic analysis of complex mycobacterial lipids. Soc Appl Bacteriol Techn Series 1985;20:237-65.  Back to cited text no. 19
Minnikin DE, Minnikin SM, Hutchinson IG, Goodfellow M, Grange JM. Mycolic acid patterns of representative strains of Mycobacterium fortuitum, 'Myobacterium peregrinum' and Mycobacterium smegmatis. J Gen Microbiol 1984;130:363-7.  Back to cited text no. 20
Velayati AA, Farnia P, Mozafari M, Mirsaeidi M. Nontuberculous mycobacteria isolation from clinical and environmental samples in Iran: Twenty years of surveillance. Biomed Res Int 2015;2015:254285.  Back to cited text no. 21
Hamid ME, Roth A, Landt O, Kroppenstedt RM, Goodfellow M, Mauch H. Differentiation between Mycobacterium farcinogenes and Mycobacterium senegalense strains based on 16S-23S ribosomal DNA internal transcribed spacer sequences. J Clin Microbiol 2002;40:707-11.  Back to cited text no. 22
Cowan ST, Steel KJ. Cowan and Steel's Manual for the Identification of Medical Bacteria. Cambridge University Press; 2003.  Back to cited text no. 23
Kent PT, Kubica GP. Public health Mycobacteriology. A Guide for the Level III Laboratory; 1985.  Back to cited text no. 24
Mordarska H, Mordarski M, Goodfellow M. Chemotaxonomic characters and classification of some nocardioform bacteria. J Gen Microbiol 1972;71:77-86.  Back to cited text no. 25
el Sanousi SM, Tag el Din MH. On the aetiology of bovine farcy in the Sudan. J Gen Microbiol 1986;132:1673-5.  Back to cited text no. 26
Hamid ME, Mohamed GE, Abu-Samra MT, el-Sanousi SM, Barri ME. Bovine farcy: A clinico-pathological study of the disease and its aetiological agent. J Comp Pathol 1991;105:287-301.  Back to cited text no. 27
Mansouri D, Mahdaviani SA, Khalilzadeh S, Mohajerani SA, Hasanzad M, Sadr S, et al. IL-2-inducible T-cell kinase deficiency with pulmonary manifestations due to disseminated Epstein-Barr virus infection. Int Arch Allergy Immunol 2012;158:418-22.  Back to cited text no. 28
Mostafa IE. Studies of bovine farcy in the Sudan. I. Pathology of the disease. J Comp Pathol 1967;77:223-9.  Back to cited text no. 29
Perpezat A, Destombes P, Mariat F. Histopathological study of the nocardiosis of beef in Chad and biochemical characteristics of Nocardia farcinica. Journal of tropical livestock science 1967;20:429-35.  Back to cited text no. 30
Salih MA, El Sanousi SM, Tag El Din HM. Predilection sites of bovine farcy lesions in sudanese cattle. Bull Anim Health Prod Afr 1978;26:168-71.  Back to cited text no. 31
El Sanousi SM, Salih MA, Mousa MT, Tag El Din MH, Ali SA. Further studies on the properties of the aetiology of bovine farcy isolated from sudanese cattle. Rev Elev Med Vet Pays Trop 1979;32:135-41.  Back to cited text no. 32
Diguimbaye-Djaibé C, Vincent V, Schelling E, Hilty M, Ngandolo R, Mahamat HH, et al. Species identification of non-tuberculous mycobacteria from humans and cattle of Chad. Schweiz Arch Tierheilkd 2006;148:251-6.  Back to cited text no. 33
Farnia P, Mohammadi F, Zarifi Z, Tabatabee DJ, Ganavi J, Ghazisaeedi K, et al. Improving sensitivity of direct microscopy for detection of acid-fast bacilli in sputum: Use of chitin in mucus digestion. J Clin Microbiol 2002;40:508-11.  Back to cited text no. 34
Farnia P, Mohammadi F, Masjedi MR, Varnerot A, Zarifi AZ, Tabatabee J, et al. Evaluation of tuberculosis transmission in tehran: Using RFLP and spoligotyping methods. J Infect 2004;49:94-101.  Back to cited text no. 35
Hamid ME-A. Classification and identification of actinomycetes associated with bovine farcy. University of Newcastle upon Tyne; 1994.  Back to cited text no. 36
Awad FI. The inter-relationship between tuberculosis and bovine farcy. J Comp Pathol 1958;68:324-30.  Back to cited text no. 37
El Nasri M. Some observations on bovine farcy. Vet Rec 1961;73:370-2.  Back to cited text no. 38
Moustafa IE. Studies on Cattle Nocardiosis” Bovine Farcy” in the Sudan. Royal Veterinary College (University of London); 1962.  Back to cited text no. 39
Shigidi MT, Mirghani T, Musa MT. Characterisation of Nocardia farcinica isolated from cattle with bovine farcy. Res Vet Sci 1980;28:207-11.  Back to cited text no. 40
Arush M, Dini A, Alio S, Moalim A. Incidenza della nocardiosi del bovino in Somalia. Boll Sci Fac Zoot Vet Univ Naz Somala 1982;3:95-9.  Back to cited text no. 41
Mémery G, Mornet P, Camara A. First authentic cases of beef farcin in French West Africa. Journal of tropical livestock science 1958;11:11-5.  Back to cited text no. 42
Mohan K. Mycobacterium senegalense from bovines in Eastern Nigeria. J Appl Bacteriol 1985;59:277-81.  Back to cited text no. 43
Alawa CB, Etukudo-Joseph I, Alawa JN. A 6-year survey of pathological conditions of slaughtered animals at Zango abattoir in Zaria, Kaduna state, Nigeria. Trop Anim Health Prod 2011;43:127-31.  Back to cited text no. 44
Wallace RJ Jr., Brown-Elliott BA, Brown J, Steigerwalt AG, Hall L, Woods G, et al. Polyphasic characterization reveals that the human pathogen Mycobacterium peregrinum type II belongs to the bovine pathogen species Mycobacterium senegalense. J Clin Microbiol 2005;43:5925-35.  Back to cited text no. 45
Wong TC, Chan WF, Tsang WL, Yeung SH, Ip FK. Mycobacterium farcinogenes infection after total hip arthroplasty. J Arthroplasty 2005;20:684-7.  Back to cited text no. 46
Oh WS, Ko KS, Song JH, Lee MY, Ryu SY, Taek S, et al. Catheter-associated bacteremia by Mycobacterium senegalense in Korea. BMC Infect Dis 2005;5:107.  Back to cited text no. 47
Brown-Elliott BA, Wallace RJ Jr. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev 2002;15:716-46.  Back to cited text no. 48
Carson LA, Cusick LB, Bland LA, Favero MS. Efficacy of chemical dosing methods for isolating nontuberculous mycobacteria from water supplies of dialysis centers. Appl Environ Microbiol 1988;54:1756-60.  Back to cited text no. 49
Halstrom S, Price P, Thomson R. Review: Environmental mycobacteria as a cause of human infection. Int J Mycobacteriol 2015;4:81-91.  Back to cited text no. 50
  [Full text]  
Schulze-Röbbecke R, Janning B, Fischeder R. Occurrence of mycobacteria in biofilm samples. Tuber Lung Dis 1992;73:141-4.  Back to cited text no. 51
Velayati AA, Farnia P, Mozafari M, Malekshahian D, Seif S, Rahideh S, et al. Molecular epidemiology of nontuberculous mycobacteria isolates from clinical and environmental sources of a metropolitan city. PLoS One 2014;9:e114428.  Back to cited text no. 52
Azadi D, Naser AD, Shojaei H. First isolation of Mycobacterium setense from hospital water. J Coast Life Med 2016;4:331-3.  Back to cited text no. 53
Velayati AA, Farnia P, Mozafari M, Malekshahian D, Farahbod AM, Seif S, et al. Identification and genotyping of Mycobacterium tuberculosis isolated from water and soil samples of a metropolitan city. Chest 2015;147:1094-102.  Back to cited text no. 54
Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988;16:1215.  Back to cited text no. 55
Aghajani J, Farnia P, Velayati AA. Impact of geographical information system on public health sciences. Biomed Biotechnol Res J 2017;1:94.  Back to cited text no. 56
  [Full text]  
Rajaei E, Hadadi M, Madadi M, Aghajani J, Ahmad MM, Farnia P, et al. Outdoor air pollution affects tuberculosis development based on geographical information system modeling. Biomed Biotechnol Res J 2018;2:39.  Back to cited text no. 57
  [Full text]  
Merza MA, Farnia P, Tabarsi P, Khazampour M, Masjedi MR, Velayati AA, et al. Anti-tuberculosis drug resistance and associated risk factors in a tertiary level TB center in Iran: A retrospective analysis. J Infect Dev Ctries 2011;5:511-9.  Back to cited text no. 58
Hamada S, Ito Y, Hirai T, Murase K, Tsuji T, Fujita K, et al. Impact of industrial structure and soil exposure on the regional variations in pulmonary nontuberculous mycobacterial disease prevalence. Int J Mycobacteriol 2016;5:170-6.  Back to cited text no. 59
  [Full text]  
Levendoglu-Tugal O, Munoz J, Brudnicki A, Fevzi Ozkaynak M, Sandoval C, Jayabose S, et al. Infections due to nontuberculous mycobacteria in children with leukemia. Clin Infect Dis 1998;27:1227-30.  Back to cited text no. 60
Rahideh S, Derakhshaninezhad Z, Farnia P, Mozafari M, Seif S, Malekshahian D, et al. Review and meta analysis of nontuberculous mycobacteria in the middle east. Int J Mycobacteriol 2015;4:149.  Back to cited text no. 61
Diagnosis and treatment of disease caused by nontuberculous mycobacteria. This official statement of the American Thoracic Society was approved by the board of directors, March 1997. Medical Section of the American Lung Association. Am J Respir Crit Care Med 1997;156:S1-25.  Back to cited text no. 62
Booth JE, Jacobson JA, Kurrus TA, Edwards TW. Infection of prosthetic arthroplasty by Mycobacterium fortuitum. Two case reports. J Bone Joint Surg Am 1979;61:300-2.  Back to cited text no. 63
Herold RC, Lotke PA, MacGregor RR. Prosthetic joint infections secondary to rapidly growing Mycobacterium fortuitum. Clin Orthop Relat Res 1987;216:183-6.  Back to cited text no. 64
Eid AJ, Berbari EF, Sia IG, Wengenack NL, Osmon DR, Razonable RR, et al. Prosthetic joint infection due to rapidly growing mycobacteria: Report of 8 cases and review of the literature. Clin Infect Dis 2007;45:687-94.  Back to cited text no. 65
Portaels F, De Muynck A, Sylla MP. Selective isolation of mycobacteria from soil: A statistical analysis approach. J Gen Microbiol 1988;134:849-55.  Back to cited text no. 66


  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3]

This article has been cited by
1 Airborne Disinfection by Dry Fogging Efficiently Inactivates Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), Mycobacteria, and Bacterial Spores and Shows Limitations of Commercial Spore Carriers
Jan Schinköthe,Hendrik A. Scheinemann,Sandra Diederich,Holger Freese,Michael Eschbaumer,Jens P. Teifke,Sven Reiche,Harold L. Drake
Applied and Environmental Microbiology. 2020; 87(3)
[Pubmed] | [DOI]


Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  In this article
Article Figures
Article Tables

 Article Access Statistics
    PDF Downloaded228    
    Comments [Add]    
    Cited by others 1    

Recommend this journal