The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 13, 2019

Isolation and Characterization of Medically Important Aerobic Actinomycetes in Soil of Iran (2006 - 2007)



Mohammad Reza Aghamirian1, Seyed Amir Ghiasian2, *
1 Medical Parasitology and Mycology Department, Qazvin University of Medical Sciences and Health Services, Qazvin, Iran
2 Medical Parasitology and Mycology Department, School of Medicine, Hamadan University of Medical Sciences and Health Services, Hamadan, Iran

Abstract

The aerobic actinomycetes are a large group of soil-inhabiting bacteria that occur worldwide. Some of them are the main cause of two important diseases, nocardiosis and actinomycetoma. To identify the prevalence and geographic distribution of aerobic actinomycetes in soil of Qazvin province, a study was carried out during 2006-2007. In this study, the incidence and diversity of medically important aerobic actinomycetes was determined in 300 soil samples of different parts of Qazvin. The suspensions of superficial soil samples were prepared by adding of normal saline, streptomycin and chloramphenicol and the supernatants were cultured on brain-heart infusion agar and Sabouraud's dextrose agar contain cycloheximide. The isolated microorganisms were examined by Gram and acid-fast stains and were identified biochemically and morphologically. Of 96 aerobic actinomycetes isolates identified, Actinomadura madurae and Streptomyces somaliensis were the most frequently isolated species each representing 19.8% of isolates, followed by Nocardia asteroides (15.6%), N. otitidiscaviarum (9.4%), N. brasiliensis (7.3%), A. peletieri, S. griseus, and Nocardia spp. (each 5.2%), and N. transvalensis, Nocardiopsis dassonvillei, Actinomadura spp. and Streptomyces spp. (each 3.1%). To the best of our knowledge, this is the first report on epidemiological investigation of medically important aerobic actinomycetes in soil samples from Iran. In recent years, mycetoma and nocardiosis have been increasingly reported in Iran. The results showed that medically important actinomycetes occur in the environment of Iran and soil could be potential source of actinomycotic infections.

Key Words: Aerobic actinomycetes, soil, Qazvin, Iran.


Article Information


Identifiers and Pagination:

Year: 2009
Volume: 3
First Page: 53
Last Page: 57
Publisher Id: TOMICROJ-3-53
DOI: 10.2174/1874285800903010053

Article History:

Received Date: 23/3/2009
Revision Received Date: 27/3/2009
Acceptance Date: 30/3/2009
Electronic publication date: 20/4/2009
Collection year: 2009

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© Aghamirian and Ghiasian; Licensee Bentham Open.

open-access license: This is an open access article licensed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited.


* Address correspondence to this author at the Medical Parasitology and Mycology Department, School of Medicine, Hamadan University of Medical Sciences and Health Services, PO Box 65155-518 Hamadan, Iran; Tel: +98- 811 8276295; Fax: +98- 811 8276299; E-mail: s.a.ghiasian@umsha.ac.ir




INTRODUCTION

Actinomycetes are found worldwide, maintaining a saprophytic existence in soil and other natural habitats. Soil is a major reservoir for retention of bacteria and fungi and wind can transmit these agents in companion with dust and dirt into lung or skin and produce diseases like nocardiosis, sporotrichosis, chromomycosis, mycetoma etc [1Anonymous. Indoor air guideline In: Department of Social Affairs and Health. Finland: Edita Helsinki 1997. (In Finnish)].

The aerobic actinomycetes are a various group of Grampositive, branching, filamentous, obligately aerobic and relatively slow-growing bacteria. Actinomycetes are considered as Spore-forming bacteria with indication of health problems [1Anonymous. Indoor air guideline In: Department of Social Affairs and Health. Finland: Edita Helsinki 1997. (In Finnish)]. It is widely recognized that aerobic actinomycetes abundantly found in soil and cause opportunistic infections in human and animals and even cause death in some occasions. It has been known that Streptomyces species can produce secondary metabolites [2Gräfe U. Biosynthesen ausgewandten Strukturklassen In: Biochemie der Antibiotika: Struktur-Biosynthese-Wirkmechanismus. Germany: Spektrum Akademischer-Verlag GmbH, Heidelberg 1992; pp. 219-318.]. Toxic metabolites isolated from Streptomyces and Nocardiopsis isolates have shown to be mitochondriotoxic in spermatozoa [3Peltola J, Andersson MA, Haahtela T, et al. Toxic-metabolite-producing bacteria and fungus in an indoor environment Appl Environ Microbiol 2001; 67: 3269-74.]. It is recognized that some isolates of Streptomyces griseus produce valinomycin, a toxin that cause mitochondrial swelling, activity loss, and apoptosis in human natural killer cells [4Andersson MA, Mikkola R, Kroppenstedt RM, et al. The mitochondrial toxin produced by Streptomyces griseus strains isolated from an indoor environment is valinomycin Appl Environ Microbiol 1998; 64: 4767-73.].

Streptomyces species may be implicated in respiratory disorders of individuals living in moldy houses [5Hirvonen M-R, Nevalainen A, Makkonen N, Mönkkönen J, Savolainen K. Streptomycetes spores from moldy houses induce nitric oxide, TNFα and IL-6 secretion from RAW 264.7 macrophage cell line without causing subsequent cell death Environ Toxicol Pharmacol 1997; 3: 57-63.]. Increase in the infections by aerobic actinomycetes, specially Nocardia genus and diverse array of clinical illnesses specially the systemic and disseminated forms of nocardiosis in cancer, tuberculosis, diabetes, AIDS and patients under treatment with immunosuppressive drugs and broad spectrum antibiotics in the world reveal importance of detection of these agents more than ever [6Saubolle MA, Sussland D. Nocardiosis: review of clinical and laboratory experience J Clin Microbiol 2003; 41: 4497-501.]. Actinomycetes present in soil like Streptomyces somaliensis, Nocardia brasiliensis, N. asteroides, Actinomadura peletieri, A. madurae also can be inoculated in the skin in a companion with dust and dirt and may cause actinomycetoma [6Saubolle MA, Sussland D. Nocardiosis: review of clinical and laboratory experience J Clin Microbiol 2003; 41: 4497-501., 7Zarei MA, Zarrin M. Mycetomas in Iran: a review article Mycopathologia 2008; 165: 135-41.]. Mycetoma and nocardiosis are sporadically spread in Iran and treatment of mycetoma essentially depends on the etiologic agent involved. In order to determine the identities and diversity of soil actinomycetes in Qazvin district of Iran, a descriptive analytical study conducted to find out if soils are potential sources of actinomycetes infections. To the best of our knowledge, this is the first report on epidemiological investigation of distribution of aerobic actinomycete populations in soil samples from Iran.

MATERIALS AND METHODOLOGY

Qazvin is a province situated on the northern west of capital, Tehran. The average summer temperature ranges from 25 to 35°C and humidity is up to 50%. Qazvin city covering an area of 50 sq. kms and has been divided into 25 regions (Fig. 1).

Fig. (1)

Map of Iran, showing relative position of Qazvin with capital and 25 regions, from which samples were collected.



Over the period of the study (March 2006 to March 2007), total 300 soil samples were collected from 25 locations of the city, that is, 12 samples were randomly taken from 350 to 400 meters interval in each region. After removing the surface loose litter layer (approximately top 4 cm), the soil samples were taken from a depth of 5 to 10 centimeters of the superficial layers in each location. The soil type was sandy-clay in all over the city. Soil samples were numbered and put in a sterilized paper sack, transferred to the Mycology Laboratory of the School of Medicine, Qazvin University of Medical Sciences, where they were homogenized and spread in trays to be cleaned of leaves, roots, small stems, etc. These samples were sieved (2 mm mesh) and air dried at 25 °C for 7 days. Then five grams of each soil sample were added to a test tube containing 10 ml of sterile physiologic saline (0.9% NaCl) and mixed for 3 minutes. The suspension was incubated for 15 minutes and thereafter, 3 ml of the supernatant solution was transferred to another sterile test tube and 1.5 ml of antibiotic solutions of streptomycin and chloramphenicol (0.2 mg/ml) was added and incubated for half an hour after being stirred up. This solution was then shaked again and one drop (0.05 ml) was added to a Sabouraud's dextrose agar medium (BioMeriéux, Marcy-1, Etoil, France), containing 0.5 g/l of cycloheximide and another drop to brain-heart infusion agar containing 0.5 g/l of cycloheximide immediately, and incubated at 35°C for 2-3 weeks. Representative colonies were selected and streaked on new plates of aforementioned culture media. Actinomycetes on the plates were identified as colored, dried, rough, with irregular/regular margin, generally convex colony. The plates were kept in a 35°C incubator and examined for up to 2 or 3 weeks for possible growing, although the majority was detected within the first several days of incubation. During this period, the wrinkled colonies of yellow, red, orange, and white to cream colors suspicious of actinomycetes were considered and in order to purification of actinomycetes, the streak plate method were used. After isolation of the pure colonies based on their colonial morphology, colour of hyphae, color of aerial mycelia, they were individually plated on the same agar media.

Morphological examination of the actinomycetes was done by using cellophane tape and cover slip-buried methods. The mycelium structure, color and arrangement of arthrospore on the mycelium were examined using light microscopy under oil immersion (1,000 x). Since a single method could not identify all actinomycete isolates to the species level; therefore, a combination of methods was necessary. If branched and delicate filaments specific of actinomycetes were seen, they were isolated and examined for partial acid-fastness by staining with the carbolfuchsin modified acid-fast stain with a weak (0.5-1%) sulfuric acid decolorizing solution. Moreover, conventional biochemical tests and physiological criteria such as the capability to degrade the organic compounds such as casein, tyrosine, xanthine, hypoxanthine and starch as substrates, the utilization of urea and different carbon sources as well as growth in 4% gelatin medium were studied in order to reach a possible classification to the species level. Gelatin hydrolysis was determined by stabbing a loopful of organism about one cm into a nutrient gelatin tube (BBL), which were incubated at 35°C in air for up to 7 days. Detection of hydrolysis was accomplished by placing the tubes at 4°C for 15 min and then tilting each tube at a 45° angle. The test was considered positive if the gelatin was liquefied. For urea hydrolysis, a heavy loopful of bacteria was suspended in 0.5 ml of a medium containing 1 g urea and 1 ml of a cresol red solution (0.5% [wt/vol]) in 100 ml phosphate buffer (0.005M, pH 6). Tubes were incubated at 35°C and checked after 1 and 2 days for a pink color shift representing a positive reaction.

RESULTS

Of 300 soil samples studied, a total of 96 actinomycete isolates, representing 9 species, were diagnosed including Nocardia asteroides, N. otitidiscaviarum (Formerly N. caviae), N. brasiliensis, N. transvalensis, Actinomadura peletieri, A. madurae, Streptomyces somaliensis, S. griseus and Nocardiopsis dassonvillei. The remaining 11 isolates were identified at the genus level including Nocardia (five isolates), and Actinomadura and Streptomyces (each 3 isolates). Table 1 shows the numbers, diversity and prevalence of the actinomycete populations in soil samples from these 25 locations. A total of 34 (35.4%) Nocardia isolates, representing four species, were identified. Of which, N. asteroides surpassed the other three species of Nocardia, accounting for 44.1% of all Nocardia species, and ranked third in prevalence (15.6% of all isolates). All Nocardia isolates exhibited partial acid-fastness, varying from weak to strong. Colony morphology of Nocardia spp. were glabrous, wrinkled or granular with color of orange, yellow to white. Regarding N. transvalensis, both of the isolates tested decomposed hypoxanthine, tyrosine, and urea and were negative for casein decomposition.

Table 1.

Prevalence and Diversity of Acinomycetes Isolated from 300 Soil Samples in Qazvin City




The Streptomyces colonies were slow growing, aerobic, folded, glabrous or chalky, with earthy odour and aerial mycelia of different colors. All streptomycete isolates were acid-fast negative and Gram-stain positive. The degradation of the substrates casein and tyrosine by S. somaliensis and S. griseus was positive but for xanthine was variable. Microscopically, it was observed that the morphology of the spore chains varied depending on the species, which was straight or flexuous, hook or coil form.

N. brasiliensis, Nocardiopsis dassonvillei, S. griseus and S. somaliensis were the species capable of liquefying gelatin. N. transvalensis and Nocardiopsis dassonvillei were the only species could breakdown starch. The percentage of species may be presented by overall rate (positive number/300 soil samples).

DISCUSSION

In this study, aerobic actinomycetes present in soil were isolated frequently from soil of different parts of Qazvin province. Actinomycetes may cause various infections such as nocardiosis and actinomycetoma, which deserve special attention but delay in diagnosis result in deterioration of the patient's condition and mortality rate, especially in cases of metastatic nocardiosis.

In the Finnish Health Authority guidelines, existence of spore-forming actinobacteria in the environments has been considered as a risk to human health [1Anonymous. Indoor air guideline In: Department of Social Affairs and Health. Finland: Edita Helsinki 1997. (In Finnish)]. The literature is crowded with case reports on actinomycotic infections especially mycetoma. Several reports from various geographical locations of Iran have shown that actinomycotic mycetoma is a sporadic disease, frequent etiological agents of which are N. asteroids and Actinomadura madura [7Zarei MA, Zarrin M. Mycetomas in Iran: a review article Mycopathologia 2008; 165: 135-41.-11Shamsadini S, Shamsi MS, Sadre ES, Vahidreza S. Report of two cases of mycetoma in the Islamic Republic of Iran East Mediterr Health J 2007; 13: 1219-22.]. In this study, out of 300 soil samples, 96 actinomycete isolates (32%) yielded, which A. madurae and S. somaliensis were of the predominant isolates (Table 1). Whereas in a study carried out in Rome, out of 200 soil samples examined, only 12 actinomycete species (6%) including seven isolates of N. asteroides, four of A. madurae and one of Nocardiopsis dassonvillei were isolated [12Polonelli L, Morace G, Barcaioli BM, Cossu AL. Survey of human pathogenic actinomycetes and fungi in soil from Rome and other Italian areas Mycopathologia 1981; 73: 161-9.]. According to a study carried out on 64 cases of actinomycetomas over 33 years in Iran, Actinomadura madurae has been the cause of 10.2% of the cases [7Zarei MA, Zarrin M. Mycetomas in Iran: a review article Mycopathologia 2008; 165: 135-41.]. Furthermore, Denguezli et al. has reported that of 10 actinomycetoma cases from Tanzania, nine cases were caused by A. madurae [13Denguezli M, Kourda M, Ghariani N, et al. Mycetoma in central Tunisia Ann Dermatol Venereol 2003; 130: 515-8.].

In this study, 40.6% of soil samples in Qazvin, contained different species of Nocardia, which is much higher than what reported in Patiala, India, that is 8% [14Goel S, Kanta S. Prevalence of Nocardia species in the soil of Patiala area Indian J Pathol Microbiol 1993; 36: 53-60.]. Nocardiae are ubiquitous in the environment and well known as saprophytic soil inhabitants. Identification of Nocardiae to the species level appears to be of significant benefit to the patients’ management and defining the geographic distribution of these organisms. Members of the genus Nocardia are most commonly associated with a diverse array of opportunistic infections in both immunocompromised and immunocompetent hosts [15Brown JM, McNeil MM. Nocardia, Rhodococcus, Gordonia, Actinomadura, Streptomyces, and other aerobic actinomycetes In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, Eds. Manual of clinical microbiology. 9th ed. Washington D.C: American Society for Microbiology 2003; pp. 502-31.]. In a study carried out during 1972 to 2005 in Iran, most of (84.5%) all mycetoma cases were actinomycetoma [7Zarei MA, Zarrin M. Mycetomas in Iran: a review article Mycopathologia 2008; 165: 135-41.], which is in concordance with the results of Dieng et al. and Denguezli et al. [13Denguezli M, Kourda M, Ghariani N, et al. Mycetoma in central Tunisia Ann Dermatol Venereol 2003; 130: 515-8.,16Dieng MT, Niang SO, Diop B, Ndiaye B. Actinomycetomas in Senegal: study of 90 cases Bull Soc Pathol Exot 2005; 98: 18-20.]. From the available data, mycetomas were abundant among farmers in rural areas of Iran and the disease mainly has been seen in foot, which shows that the causative agents mostly implanted from soil or plants traumatically [7Zarei MA, Zarrin M. Mycetomas in Iran: a review article Mycopathologia 2008; 165: 135-41., 8Griffith WA, Kohout E, Vessal K. Mycetoma in Iran Int J Dermatol 1975; 14: 209-13., 10Ravaghi M, Aflatouni M. Mycetoma caused by Nocardia asteroides J Pak Med Assoc 1978; 28: 35-6.]. Similar results have been found in Argentina [17Negroni R, Lopez DG, Arechavala A, Bianchi MH, Robles AM. Clinical and microbiological study of mycetomas at the Muniz hospital of Buenos Aires between 1989 and 2004 Rev Argent Microbiol 2006; 38: 13-8.] and Tanzania [13Denguezli M, Kourda M, Ghariani N, et al. Mycetoma in central Tunisia Ann Dermatol Venereol 2003; 130: 515-8.].

Most of the nocardiosis cases are caused by N. asteroides [15Brown JM, McNeil MM. Nocardia, Rhodococcus, Gordonia, Actinomadura, Streptomyces, and other aerobic actinomycetes In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, Eds. Manual of clinical microbiology. 9th ed. Washington D.C: American Society for Microbiology 2003; pp. 502-31.] and in the current study, this species surpassed the other Nocardia species and had allowed it to become the most common Nocardia species isolated from soil. These results are comparable with those of the Kuwaiti and Italian studies [12Polonelli L, Morace G, Barcaioli BM, Cossu AL. Survey of human pathogenic actinomycetes and fungi in soil from Rome and other Italian areas Mycopathologia 1981; 73: 161-9., 18Khan ZU, Neil L, Chandy R, et al. Nocardia asteroides in the soil of Kuwait Mycopathologia 1997; 137: 159-63.]. Nocardiae are usually acquired through inhalation and infrequently by direct skin inoculation [15Brown JM, McNeil MM. Nocardia, Rhodococcus, Gordonia, Actinomadura, Streptomyces, and other aerobic actinomycetes In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, Eds. Manual of clinical microbiology. 9th ed. Washington D.C: American Society for Microbiology 2003; pp. 502-31.]. A study from South India showed that contact with soil and sands contaminated with N. asteroides has been the reason for 1.4% of corneal lesions cases [19Bharathi MJ, Ramakrishnan R, Vasu S, Meenakshi CA, Palaniappan R. Nocardia asteroides keratitis in South India Indian J Med Microbiol 2003; 21: 31-6.]. Nocardiosis produced by Nocardia spp. present in soil were unusual in the past, but they are in increase in recent years with the increase in the number of immune deficiency patients [20Shivaprakash MR, Rao P, Mandal J, et al. Nocardiosis in a tertiary care hospital in North India and review of patients reported from India Mycopathologia 2007; 163: 267-74.]. Curry (1980] stated that 38 percent of people inflicted with pulmonary nocardiosis lacked any background [21Curry WS. Human nocardiosis: a clinical review with selected case reports Arch Intern Med 1980; 140: 816-.]. Different forms of Nocardiosis in various immunocompromised patients have been recognized in Iran [personal communication]. Over the past decades in Iran, the frequency of pulmonary nocardiosis infections caused by N. asteroides has increased [22Asilian A, Yoosefi A, Faghihi G. Cutaneous and pulmonary nocardiosis in pemphigus vulgaris: a rare complication of immunosuppressive therapy Int J Dermatol 2006; 45: 1204-6.-25Eshraghi S, Amin M. Nocardia asteroides complex in patients with symptomatic pulmonary nocardiosis Iran J Public Health 2001; 30: 99-102.]. These patients typically had predisposing factors such as pemphigus vulgaris, kidney transplantation, chronic lymphocytic leukemia and Wagner vasculitis. According to Munoz et al. [26Muñoz J, Mirelis B, Aragón LM, et al. Clinical and microbiological features of nocardiosis 1997-2003 J Med Microbiol 2007; 56: 545-0.], N. asteroides and N. brasiliensis have been the most common agents of nocardiosis in HIV-positive patients.

In this study, N. otitidiscaviarum was the second most prevalent Nocardia spp. and was accounted for 26.7% of all Nocardia species, but based on the literature, this species has infrequently been recovered from soil throughout the world. It has also been postulated that N. otitidiscaviarum is less pathogenic than other species of Nocardia [27Clark NM, Braun DK, Pasternak A, Chenoweth CE. Primary cutaneous Nocardia otitidiscaviarum infection: case report and review Clin Infect Dis 1995; 20: 1266-70.] and represented only between 1.3 and 4.8% of clinical Nocardia isolates in the studies from Europe, Japan and the USA [28Forster DH, Becker A, Kniehl E. Severe pulmonary Nocardia otitidiscaviarum infection in a patient with underlying chronic lung disease and long-term corticosteroid therapy, confirmed by 16S rRNA gene sequencing In: 15th European Congress of Clinical Microbiology and Infectious Diseases; April 2-5; Copenhagen / Denmark. 2005. Abstract number: 1135-122]. Based on a study on 264 actinomycetoma patients from west of Bengal, N. otitidiscaviarum has had a lower incidence of etiological agents [29Maiti PK, Ray A, Bandyopadhyay S. Epidemiological aspects of mycetoma from a retrospective study of 264 cases in West Bengal Trop Med Int Health 2002; 7: 788-92.].

In our study, Nocardia brasiliensis constituted 20.6% of all Nocardia species. This Nocardia species produces infection most frequently in immunocompromised patients, but it can cause cutaneous and disseminated infection in immunocompetent patients too [30Callen JP, Kingman J. Disseminated cutaneous Nocardia brasiliensis infection Pediatr Dermatol 1984; 2: 49-51.]. A review of actinomycetomas cases from 1972 to 2005 in Iran demonstrated that N. brasiliensis has been the cause of 86.6% of the cases, which have mostly been associated with tropical environments [7Zarei MA, Zarrin M. Mycetomas in Iran: a review article Mycopathologia 2008; 165: 135-41.]. In the United States also, N. brasiliensis is the second most common isolate of Nocardia [6Saubolle MA, Sussland D. Nocardiosis: review of clinical and laboratory experience J Clin Microbiol 2003; 41: 4497-501.].

In the current study, N. transvalensis and Nocardiopsis dassonvillei were the uncommon (each 3.1%) actinomycete species isolated. It has been stated that the specific natural habitat of N. transvalensis has not yet been identified [6Saubolle MA, Sussland D. Nocardiosis: review of clinical and laboratory experience J Clin Microbiol 2003; 41: 4497-501.]. Nocardiopsis species have been observed in indoor environments and shown to produce antimicrobial and bioactive agents. Nocardiopsis dassonvillei isolated from lung biopsies of farmers suffering from alveolitis [3Peltola J, Andersson MA, Haahtela T, et al. Toxic-metabolite-producing bacteria and fungus in an indoor environment Appl Environ Microbiol 2001; 67: 3269-74.].

This is the first report on isolation and characterization of medically important aerobic actinomycetes in soil of Iran. This study can possibly reveal actinomycetes agents that engaged in actinomycotic diseases in Iran. Familiarity with the epidemiology of unusual Nocardia species may increase early identification in cases of nocardial infection. Moreover, it is obvious that efforts for the isolation, characterization and study on actinomycetes from different ecological niches can be a milestone for the discovery of novel species that may yield potential human and veterinary pathogens.

ACKNOWLEDGMENTS

We are grateful to Dr. A. H. Maghsood for revising the manuscript.

REFERENCES

[1] Anonymous. Indoor air guideline In: Department of Social Affairs and Health. Finland: Edita Helsinki 1997. (In Finnish)
[2] Gräfe U. Biosynthesen ausgewandten Strukturklassen In: Biochemie der Antibiotika: Struktur-Biosynthese-Wirkmechanismus. Germany: Spektrum Akademischer-Verlag GmbH, Heidelberg 1992; pp. 219-318.
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[4] Andersson MA, Mikkola R, Kroppenstedt RM, et al. The mitochondrial toxin produced by Streptomyces griseus strains isolated from an indoor environment is valinomycin Appl Environ Microbiol 1998; 64: 4767-73.
[5] Hirvonen M-R, Nevalainen A, Makkonen N, Mönkkönen J, Savolainen K. Streptomycetes spores from moldy houses induce nitric oxide, TNFα and IL-6 secretion from RAW 264.7 macrophage cell line without causing subsequent cell death Environ Toxicol Pharmacol 1997; 3: 57-63.
[6] Saubolle MA, Sussland D. Nocardiosis: review of clinical and laboratory experience J Clin Microbiol 2003; 41: 4497-501.
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[12] Polonelli L, Morace G, Barcaioli BM, Cossu AL. Survey of human pathogenic actinomycetes and fungi in soil from Rome and other Italian areas Mycopathologia 1981; 73: 161-9.
[13] Denguezli M, Kourda M, Ghariani N, et al. Mycetoma in central Tunisia Ann Dermatol Venereol 2003; 130: 515-8.
[14] Goel S, Kanta S. Prevalence of Nocardia species in the soil of Patiala area Indian J Pathol Microbiol 1993; 36: 53-60.
[15] Brown JM, McNeil MM. Nocardia, Rhodococcus, Gordonia, Actinomadura, Streptomyces, and other aerobic actinomycetes In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, Eds. Manual of clinical microbiology. 9th ed. Washington D.C: American Society for Microbiology 2003; pp. 502-31.
[16] Dieng MT, Niang SO, Diop B, Ndiaye B. Actinomycetomas in Senegal: study of 90 cases Bull Soc Pathol Exot 2005; 98: 18-20.
[17] Negroni R, Lopez DG, Arechavala A, Bianchi MH, Robles AM. Clinical and microbiological study of mycetomas at the Muniz hospital of Buenos Aires between 1989 and 2004 Rev Argent Microbiol 2006; 38: 13-8.
[18] Khan ZU, Neil L, Chandy R, et al. Nocardia asteroides in the soil of Kuwait Mycopathologia 1997; 137: 159-63.
[19] Bharathi MJ, Ramakrishnan R, Vasu S, Meenakshi CA, Palaniappan R. Nocardia asteroides keratitis in South India Indian J Med Microbiol 2003; 21: 31-6.
[20] Shivaprakash MR, Rao P, Mandal J, et al. Nocardiosis in a tertiary care hospital in North India and review of patients reported from India Mycopathologia 2007; 163: 267-74.
[21] Curry WS. Human nocardiosis: a clinical review with selected case reports Arch Intern Med 1980; 140: 816-.
[22] Asilian A, Yoosefi A, Faghihi G. Cutaneous and pulmonary nocardiosis in pemphigus vulgaris: a rare complication of immunosuppressive therapy Int J Dermatol 2006; 45: 1204-6.
[23] Mooraki A, Jenabi A, Bastani B. Resolution of pulmonary and cerebral nocardiosis in renal transplant patient despite continued immunosuppression: a case report Transplant Proc 2003; 35: 2694-5.
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[26] Muñoz J, Mirelis B, Aragón LM, et al. Clinical and microbiological features of nocardiosis 1997-2003 J Med Microbiol 2007; 56: 545-0.
[27] Clark NM, Braun DK, Pasternak A, Chenoweth CE. Primary cutaneous Nocardia otitidiscaviarum infection: case report and review Clin Infect Dis 1995; 20: 1266-70.
[28] Forster DH, Becker A, Kniehl E. Severe pulmonary Nocardia otitidiscaviarum infection in a patient with underlying chronic lung disease and long-term corticosteroid therapy, confirmed by 16S rRNA gene sequencing In: 15th European Congress of Clinical Microbiology and Infectious Diseases; April 2-5; Copenhagen / Denmark. 2005. Abstract number: 1135-122
[29] Maiti PK, Ray A, Bandyopadhyay S. Epidemiological aspects of mycetoma from a retrospective study of 264 cases in West Bengal Trop Med Int Health 2002; 7: 788-92.
[30] Callen JP, Kingman J. Disseminated cutaneous Nocardia brasiliensis infection Pediatr Dermatol 1984; 2: 49-51.

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Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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