The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 13, 2019
RESEARCH ARTICLE

Etiological Trends and Patterns of Antimicrobial Resistance in Respiratory Infections



Salma M. Al-Zain Ahmed1, *, Sara S. Abdelrahman1, Doua M. Saad1, Isra S. Osman1, Modasir G. Osman2, Eltahir A. G. Khalil1
1 Institute of Endemic Diseases, University of Khartoum, Khartoum, Sudan
2 Elzahrawi medical laboratory, Khartoum, Khartoum, Sudan

Abstract

Background:

Respiratory infections are one of the commonest causes of morbidity and mortality related to infectious diseases worldwide. The emergence of antimicrobial resistance is a major global health problem which is well established in developing countries. Good clinical suspicion and correct laboratory identification of respiratory infection causing organisms followed by the appropriate management are needed to compact both community-acquired and nosocomial infection respiratory infections.

Objectives:

A retrospective study was carried out to elucidate the etiology of respiratory infections in Sudan, as well as to guide the physician to the best antimicrobial alternatives used in the treatment of respiratory infection.

Method:

Respiratory isolates that have been morphologically identified and biologically characterized were subjected to antibiotic susceptibility testing.

Results:

A total of 1481 respiratory specimens were examined, recovering 377 organisms from 350 culture positive samples [225(59.7%) sputum, 94(24.9%) broncho-alveolar lavage (BAL), 58(15.4%) Pleural fluid], the commonest organisms were Klebsiella ssp. (25.20%) and mycobacterium tuberculosis (25.20%), followed by Staphylococcus aureus(19.89%) and Pseudomonas aeruginosa(8.49%). High rate of resistance of bacterial isolates was observed to Co-trimoxazole (BA), Ampicillin sulbactam (AS), Cefotaxime (CF) and Tetracycline (TE), being 80%, 72.3%, 68.8% and 66.9% respectively; on the other hand, very low resistance rate was found to Amikacin (AK) and Levofloxacin (LE), being 4.6% and 8.5%, respectively.

Conclusion:

Guided prescription of antimicrobial agents must be implemented and controlled to limit further spread of antimicrobial resistance.

Keywords: Etiological trends, Antimicrobial Resistance, Respiratory Infections, Morbidity, Mortality, Nosocomial infection.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 12
First Page: 34
Last Page: 40
Publisher Id: TOMICROJ-12-34
DOI: 10.2174/1874285801812010034

Article History:

Received Date: 22/11/2017
Revision Received Date: 16/03/2018
Acceptance Date: 19/03/2018
Electronic publication date: 30/03/2018
Collection year: 2018

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© 2018 Ahmed et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Institute of Endemic Diseases, University of Khartoum, Khartoum, Sudan; Tel: +249927790916; E-mail: salmamed13@yahoo.com




1. INTRODUCTION

Infection of the respiratory tract is regarded as the most common infection among humans worldwide [1Carroll KC. Laboratory diagnosis of lower respiratory tract infections: controversy and conundrums J Clin Microbiol 2002; 40(9): 3115-20.[http://dx.doi.org/10.1128/JCM.40.9.3115-3120.2002] [PMID: 12202540] ]. Respiratory infections are a persistent health problem and being a common reason for consultation and hospitalization, impose an enormous burden on society. The clinical features of respiratory infection differ according to age, sex and co-morbidities [2Mishra SK, Kathel HP, Acharya J, Shah NP, Shah AS, Sherchand JB, et al. Recent trends of bacterial aetiology of LRTI in Nepal. Int J Infect Microbial 2012; 1(1): 3-8.]. Respiratory infection constituted for 34.6% of reported deaths in the southeast area and out of the total 3,941,000 deaths worldwide [3Leading causes of deaths in the SEA Region and the World Health Situation in the South East Asia Region 1998-2000 2002.].

Respiratory infection is a major health problem representing over 50 million deaths per year attributed to both community-acquired and nosocomial infection [4Zafar A, Hussain Z, Lomama E, Sibiie S, Irfan S, Khan E. Antibiotic susceptibility of pathogens isolated from patients with community-acquired respiratory tract infections in Pakistan- the active study. J Ayub Med Coll Abbottabad 2008; 20(1): 7-9.], furthermore respiratory diseases accounted for 13.3% of Disability–Adjusted Life Years (DALYs) [5World Health Organization. Disease Burden and Economics. Practical Approach to Lung Health (PAL). WHO. Ayub Med Coll Abbottabad 2003; 20(1): 7-9.]. The etiological agents of respiratory infections vary from area to another as well as their antibiotics susceptibility [6Ozyilmaz E, Akan OA, Gulhan M, Ahmed K, Nagatake T. Major bacteria of community-acquired respiratory tract infections in Turkey. Jpn J Infect Dis 2005; 58(1): 50-2.[PMID: 15728995] ]. Among the common bacterial causes of respiratory infections are Streptococcus, Klebsiella, Pseudomonas, Staphylococcus and Haemophilus influenza [7Siddalingappa CM. Sensitivity pattern of bacteria causing respiratory tract infections in a tertiary care centre. Int J Basic Clin Pharmacol 2013; 2(5): 590-5.[http://dx.doi.org/10.5455/2319-2003.ijbcp20131015] ]. However, the responsible pathogens are not identified in 50% of the patients despite thorough diagnostic tests are carried out [8Akter S, Shamsuzzaman SM, Jahan F. Community acquired bacterial pneumonia: aetiology, laboratory detection and antibiotic susceptibility pattern. Malays J Pathol 2014; 36(2): 97-103.[PMID: 25194532] ]. Physicians usually rely on clinical signs and symptoms to diagnose respiratory infections; the microbial etiology is rarely identified [9Macfarlane J, Holmes W, Gard P, et al. Prospective study of the incidence, aetiology and outcome of adult lower respiratory tract illness in the community. Thorax 2001; 56(2): 109-14.[http://dx.doi.org/10.1136/thorax.56.2.109] [PMID: 11209098] ]. Recommendations of therapy are based on the severity of illness; the probabilities of the pathogens in specific geographical areas, resistance patterns of the most commonly implicated etiological agents and co-morbidities [10Bartlett JG, Dowell SF, Mandell LA, File TM Jr, Musher DM, Fine MJ. Practice guidelines for the management of community-acquired pneumonia in adults. Clin Infect Dis 2000; 31(2): 347-82.[http://dx.doi.org/10.1086/313954] [PMID: 10987697] ].

Tuberculosis is a major health problem, nine million new cases of TB and 1.4 million deaths occurred worldwide in 2011. Resistance of Mycobacterium tuberculosis to commonly used antituberclus agents is increasing, this adds to the tuberculosis burden [11 World Health Organization. Global Tuberculosis Report 2012 WHO/HTM/TB/20126 2012.]. High incidence ranks Sudan among the high prevalence countries for TB, accounting for 14.6% of the total TB burden [12WHO, Global Tuberculosis Control Surveillance, Planning, Financing, Geneva, Switzerland, 2007. WHO/HTM/TB/ 2007.376.]

The misuse of antibiotics is considered as a direct cause of antibiotic resistance worldwide. Half of the dispensed antibiotics are not truly needed [13Centers for Disease Control and Prevention (CDC). Antibiotic resistance threats in the United States, 2013.http://www.cdc.gov/drugresistance/ threat-report-2013/pdf/ar-threats-2013-508.pdf].The increased use of over the counter antibiotics not only produces resistance at the individual level but can also threaten the whole community [14Bell Brian G, Schellevis Francois, Stobberingh Ellen, Goossens Herman, Pringle Mike, et al. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance BMC Infectious Diseases 2014.http://www.biomedcentral.com/1471-2334/14/13[http://dx.doi.org/10.1186/1471-2334-14-13] ].

Antimicrobials should only be prescribed judiciously as the selective pressure on antimicrobial use inevitably leads to increased resistance of the community [15Gjelstad S, Dalen I, Lindbaek M. GPs’ antibiotic prescription patterns for respiratory tract infections--still room for improvement. Scand J Prim Health Care 2009; 27(4): 208-15.[http://dx.doi.org/10.3109/02813430903438718] [PMID: 19929185] ].

Monitoring of antimicrobial susceptibility profile and regulating dispensing of antimicrobials could be effective tools to prevent the spread of antimicrobial resistance [16Brookes-Howell L, Hood K, Cooper L, et al. Clinical influences on antibiotic prescribing decisions for lower respiratory tract infection: A nine country qualitative study of variation in care. BMJ Open 2012; 2(3): e000795.[http://dx.doi.org/10.1136/bmjopen-2011-000795] [PMID: 22619265] -19Okeke IN. Poverty and root causes of resistance in developing countries, in antimicrobial resistance in developing countries, A.d.J. Sosa, et al., Editors. 2010, Springer Science+Business Media: New York.]. Knowledge of agents causing respiratory infections and their antimicrobial profile in Sudan is meager; such information is an important determinant of patient´s treatment. Hence the present study is concerned about the identification of common pathogens causing respiratory infections in Sudan and their pattern of resistance to antimicrobial agents.

2. MATERIALS AND METHODS

2.1. Study Population

In the present study, a total number of 1481 respiratory samples were collected. The study was carried out for 6 years duration (2009 – 2015), at Elzahrawi medical laboratory-Khartoum state-Sudan, which is a reference laboratory, receives patients from Khartoum & outside of it.

2.2. Specimen Collection

All specimens were collected under possible sterile conditions, sputum samples were collected in labeled sterile containers and taken to the laboratory immediately. Bronchoalveolar lavage was obtained by infusion of 20 ml of normal saline solution to bronchial tree, which was then aspirated using fiberoptic bronchoscope. A local anesthetic (lidocaine) was injected into epidermis and parietal pleura, and then another larger gauge needle was inserted into pleural space to withdraw the pleural fluid.

2.3. The Microbiological Evaluation

The respiratory samples were inoculated on Mc Conkey, Chocolate and Blood agar (HIMEDIA©) using sterile wire loop; the inoculums were streaked out on the plates, incubated for 24 hours at 37°C and monitored for colonies formation. All isolated bacteria were examined using morphological and biochemical tests following the standard procedure described by Monica Cheesbrough [20Cheesbrough M. Monica Cheesbrough ,District Laboratory Practice in Tropical Countries Part 2 ed 2nd. 2005.ed 2nd.]. Samples that are positive for acid and alcohol fast bacilli were referred for a specialized center for culture and sensitivity.

2.4. Antimicrobial Susceptibility Testing

Antimicrobial susceptibility was carried out through disk diffusion method (modified Kirby-Bauer method) [20Cheesbrough M. Monica Cheesbrough ,District Laboratory Practice in Tropical Countries Part 2 ed 2nd. 2005.ed 2nd.]; disks were obtained from HIMEDIA and AXIOM companies. Antimicrobial agents tracked include: penicillins (penicillin G, amoxicillin/clavulanate, ampicillin/ sulbactam, piperacillin/tazobactam), cephalosporins (cefalexin, cefuroxime, ceftriaxone, ceftazidime, cefoxitin and cefalothin), monobactams (aztreonam), carbapenems (imipenem and meropenem), aminoglycosides (amikacin, gentamycin, lincomycin and streptomycin), fluoroquinolones (ciprofloxacin, norfloxacin, ofloxacin, gatifloxacin, sparfloxacin, pefloxacin, and levofloxacin), sulfonamides (cotrimoxazole), macrolides (erythromycin, roxithromycin), lincomycins (clindamycin),and glycopeptides (vancomycin).

2.5. Analytical Tools

Data were analyzed using the Epi Info 7; figures and tables were drawn using Microsoft Excel and Microsoft word.

3. RESULT

Out of 1481 specimens examined, 377organisms recovered from 350 culture positive samples, 225(59.7%), 94(24.9%), 58(15.4%) organisms recovered from sputum, broncho-alveolar lavage (BAL) and Pleural fluid respectively. Male to female ratio was 1.6: 1 (61.8% of cases were males, while 38.2% were females). Using Gram-stain, 52.69% of bacterial isolates were found to be Gram-negative while 47.31% of isolates were Gram-positive (Fig. 1). The commonest organisms were Klebsiella (25.2%) & Mycobacterium tuberculosis (25.2%) followed by Staph aureus(19.89%) and Pseudomonas(8.5%) as shown in Table (1).

Fig. (1)
Percentages of gram positive and gram negative bacteria.


Table 1
Frequencies of organisms recovered from respiratory specimens.


4. DISCUSSION

Out of 1481 samples analyzed, 377 organisms recovered from 350 (23.6%) positive cultures, leaving great number of negative results (1131) (76.4%), which could be attributed to another etiology such as a viral agent or may be due to prior use of the antibiotics.

In the present study, males were 233 (61.8%) and females were 144 (38.2%). The male predominance could be attributed to increasing incidence of smoking and alcohol consumption among males as reported in other studies [21Ziyade N. Aysegul Yagci Improving sputum culture results for diagnosis of lower respiratory tract by saline washing. Marmara Med J 2010; 23(1): 30-6., 22Egbe CA, Ndiokwere C, Omoregie R. Microbiology of lower respiratory tract infections in benin city, Nigeria. Malays. J. Med. Sci. 2011; 18(2): 27-31.[PMID: 22135583] ], or probably because females have less access to health care in our country.

Among the bacterial isolates, Klebsiella pneumoniae (25.2%) was found to be the predominant organism; the results presented in this paper are in line with those presented in several other papers in India & Nigeria [23Tripathi Purti C. Dhote Kiran. Lower respiratory tract infections: Current etiological trends and antibiogram. J Pharm Biomed Sci 2014; 04(03): 249-55.-25Taura DW, Hassan A, Yayo AM, Takalmawa H. Bacterial isolates of the respiratory tract infection and their current sensitivity pattern among patients attending Aminu Kano Teaching Hospital Kano Nigeria. Int Res J Microbiol 2013; 4(9): 226-31.]. Gram negative bacteria predominated the organisms in this study, similar to the results of H. Farida et al. [26Farida H, Gasem MH, Suryanto A, et al. Viruses and Gram-negative bacilli dominate the etiology of community-acquired pneumonia in Indonesia, a cohort study. Int J Infect Dis 2015; 38: 101-7.[http://dx.doi.org/10.1016/j.ijid.2015.07.023] [PMID: 26255889] ]. Detection of mycobacterium tuberculosis was observed to be high. Candida pneumonia was observed to be rare. The presence of Candida in sputum or other respiratory tract specimens can be caused by long term antibiotic use, immune suppression secondary to diabetes mellitus or prolonged steroid therapy [27Taschdjian CL, Kozinn PJ, Toni EF. Opportunistic yeast infections, with special reference to candidiasis. Ann N Y Acad Sci 1970; 174(2): 606-22.[http://dx.doi.org/10.1111/j.1749-6632.1970.tb45586.x] [PMID: 5278139] , 28Pillary VKG, Wilson DM, Ing TS, Kark RM. Fungus infections in steroid treated SLE. J Am Assoc 1968; 205: 261-5.[http://dx.doi.org/10.1001/jama.1968.03140310019004] ], or often represents contamination [29Blaschke S, Don M, Schillinger W, Rüchel R. Candida pneumonia in patients without definitive immunodeficiency. Mycoses 2002; 45(Suppl. 3): 22-6.[http://dx.doi.org/10.1111/j.1439-0507.2002.tb04764.x] [PMID: 12690966] ].

The lowest resistance of bacterial isolates was observed to Amikacin (4.6%) and Levofloxacin (8.5%) Table (2), with very low resistance to Amikacin documented in hospital-based study in Egypt [30Abdelaziz S. Antimicrobial resistance pattern of some bacterial pathogens involved in lower respiratory tract infections in Egypt ACTA MICROBIOLOGICA ISSN 2386-7469 2015; 1(1): 22-6.[http://dx.doi.org/10.3823/286] ]. On the other hand, high rate of resistance of bacterial isolates was observed to Co-trimoxazole (BA), Ampicillin sulbactam (AS), Cefotaxime (CF) and Tetracycline (TE): 80%, 72.3%, 68.8% and 66.9% respectively Table (2). Our results were in concordance with Victor et al. who reported high resistance of respiratory isolates from Nigeria to AS and BA [31Onuoha S. Prevalence and antibiotic sensitivity of bacterial agents involved in lower respiratory tract infections. Int J. Biol. Chem. Sci. 2011; 5(2): 774-81.]. The present study showed 90.5%(76/84) and 100%(28/28) resistance of Klebsiella and Pseudomonas aeruginosa positive isolates to cephalosporins (namely cefotaxime) respectively; this could support intrinsic resistance.

Table 2
Percentages of resistant isolates to listed antibiotics.


Fig. (2)
Distribution of organisms throughout the years (2009-2015).


Increasing rate of antibiotic resistance throughout the years could be explained by an increase in the consumption of antibiotics. Many studies proved the association between antimicrobial consumption and bacterial resistance [32Bergman M. Association between antimicrobial consumption and resistancein Escherichia coli .antimicrobial agents and chemotherapy, American Society for Microbiology Mar.2009; 912-7.]. Some antibiotics become sensitive again in later years (Figs. 3 , 4 and 5), this support the fact that rotation between antibiotic classes reduces the emergence of resistance [33Salah I. Optimizing antimicrobial drug use in surgery: an intervention strategy in a Sudanese hospital to combat the emergence of bacterial resistant. Elixir Pharmacy 2011; 41: 5657-63.].

Fig. (3)
Resistance rate of commonly used antibiotics throughout the years (2009-2015).


Fig. (4)
Resistance rate of commonly used antibiotics throughout the years (2009-2015).


Fig. (5)
Resistance rate of commonly used antibiotics throughout the years (2009-2015).


CONCLUSION AND RECOMMENDATIONS

In this study, a high level of resistance to antibiotics was observed. This problem indicates the importance of performing antibiotic susceptibility testing before empirical therapy.

Guided prescription of antimicrobial therapy should be implemented to limit the fast spread of antimicrobial resistance. Public awareness should also be raised to prohibit the widespread antibiotics misuse and to highlight the importance of hygienic practices.

Use of antibiotic cycling policy, as rotation of antibiotic classes, reduces the emergence of resistant organisms.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Ethical approval was obtained from Elzahrawi medical laboratory.

HUMAN AND ANIMAL RIGHTS

Animals did not participate in this research. All human research procedures followed were in accordance with the ethical standards of the committee responsible for human experimentation (institutional and national), and with the Helsinki Declaration of 1975, as revised in 2008.

CONSENT FOR PUBLICATION

The date of respiratory samples and antimicrobial profile belongs to Elzahrawi medical laboratory and it was documented as part of routine work so written informed consent was not obtained. Patients’ names were removed prior to data analysis.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

The authors would thank all the staff members of Elzahrawi medical laboratory for their cooperation. Special thanks to Mr. Osama and Mr. Alaa who participated in data retrieval.

REFERENCES

[1] Carroll KC. Laboratory diagnosis of lower respiratory tract infections: controversy and conundrums J Clin Microbiol 2002; 40(9): 3115-20.[http://dx.doi.org/10.1128/JCM.40.9.3115-3120.2002] [PMID: 12202540]
[2] Mishra SK, Kathel HP, Acharya J, Shah NP, Shah AS, Sherchand JB, et al. Recent trends of bacterial aetiology of LRTI in Nepal. Int J Infect Microbial 2012; 1(1): 3-8.
[3] Leading causes of deaths in the SEA Region and the World Health Situation in the South East Asia Region 1998-2000 2002.
[4] Zafar A, Hussain Z, Lomama E, Sibiie S, Irfan S, Khan E. Antibiotic susceptibility of pathogens isolated from patients with community-acquired respiratory tract infections in Pakistan- the active study. J Ayub Med Coll Abbottabad 2008; 20(1): 7-9.
[5] World Health Organization. Disease Burden and Economics. Practical Approach to Lung Health (PAL). WHO. Ayub Med Coll Abbottabad 2003; 20(1): 7-9.
[6] Ozyilmaz E, Akan OA, Gulhan M, Ahmed K, Nagatake T. Major bacteria of community-acquired respiratory tract infections in Turkey. Jpn J Infect Dis 2005; 58(1): 50-2.[PMID: 15728995]
[7] Siddalingappa CM. Sensitivity pattern of bacteria causing respiratory tract infections in a tertiary care centre. Int J Basic Clin Pharmacol 2013; 2(5): 590-5.[http://dx.doi.org/10.5455/2319-2003.ijbcp20131015]
[8] Akter S, Shamsuzzaman SM, Jahan F. Community acquired bacterial pneumonia: aetiology, laboratory detection and antibiotic susceptibility pattern. Malays J Pathol 2014; 36(2): 97-103.[PMID: 25194532]
[9] Macfarlane J, Holmes W, Gard P, et al. Prospective study of the incidence, aetiology and outcome of adult lower respiratory tract illness in the community. Thorax 2001; 56(2): 109-14.[http://dx.doi.org/10.1136/thorax.56.2.109] [PMID: 11209098]
[10] Bartlett JG, Dowell SF, Mandell LA, File TM Jr, Musher DM, Fine MJ. Practice guidelines for the management of community-acquired pneumonia in adults. Clin Infect Dis 2000; 31(2): 347-82.[http://dx.doi.org/10.1086/313954] [PMID: 10987697]
[11] World Health Organization. Global Tuberculosis Report 2012 WHO/HTM/TB/20126 2012.
[12] WHO, Global Tuberculosis Control Surveillance, Planning, Financing, Geneva, Switzerland, 2007. WHO/HTM/TB/ 2007.376.
[13] Centers for Disease Control and Prevention (CDC). Antibiotic resistance threats in the United States, 2013.http://www.cdc.gov/drugresistance/ threat-report-2013/pdf/ar-threats-2013-508.pdf
[14] Bell Brian G, Schellevis Francois, Stobberingh Ellen, Goossens Herman, Pringle Mike, et al. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance BMC Infectious Diseases 2014.http://www.biomedcentral.com/1471-2334/14/13[http://dx.doi.org/10.1186/1471-2334-14-13]
[15] Gjelstad S, Dalen I, Lindbaek M. GPs’ antibiotic prescription patterns for respiratory tract infections--still room for improvement. Scand J Prim Health Care 2009; 27(4): 208-15.[http://dx.doi.org/10.3109/02813430903438718] [PMID: 19929185]
[16] Brookes-Howell L, Hood K, Cooper L, et al. Clinical influences on antibiotic prescribing decisions for lower respiratory tract infection: A nine country qualitative study of variation in care. BMJ Open 2012; 2(3): e000795.[http://dx.doi.org/10.1136/bmjopen-2011-000795] [PMID: 22619265]
[17] Whaley LE, Businger AC, Dempsey PP, Linder JA. Visit complexity, diagnostic uncertainty, and antibiotic prescribing for acute cough in primary care: A retrospective study. BMC Fam Pract. 2013; 14: 120.[http://dx.doi.org/10.1186/1471-2296-14-120] [PMID: 23957228]
[18] King PT, MacDonald M, Bardin PG. Bacteria in COPD; their potential role and treatment. Transl Respir Med 2013; 1(1): 13.[http://dx.doi.org/10.1186/2213-0802-1-13] [PMID: 27234394]
[19] Okeke IN. Poverty and root causes of resistance in developing countries, in antimicrobial resistance in developing countries, A.d.J. Sosa, et al., Editors. 2010, Springer Science+Business Media: New York.
[20] Cheesbrough M. Monica Cheesbrough ,District Laboratory Practice in Tropical Countries Part 2 ed 2nd. 2005.ed 2nd.
[21] Ziyade N. Aysegul Yagci Improving sputum culture results for diagnosis of lower respiratory tract by saline washing. Marmara Med J 2010; 23(1): 30-6.
[22] Egbe CA, Ndiokwere C, Omoregie R. Microbiology of lower respiratory tract infections in benin city, Nigeria. Malays. J. Med. Sci. 2011; 18(2): 27-31.[PMID: 22135583]
[23] Tripathi Purti C. Dhote Kiran. Lower respiratory tract infections: Current etiological trends and antibiogram. J Pharm Biomed Sci 2014; 04(03): 249-55.
[24] Ramana KV. Anand Kalaskar Mohan Rao and Sanjeev D Rao aetiology and antimicrobial susceptibility patterns of lower respiratory tract infections (LRTI’s) in a rural tertiary care teaching hospital at karimnagar, south india. Am J Inf Dis & Microb 2013; 1(5): 101-5.[http://dx.doi.org/10.12691/ajidm-1-5-5]
[25] Taura DW, Hassan A, Yayo AM, Takalmawa H. Bacterial isolates of the respiratory tract infection and their current sensitivity pattern among patients attending Aminu Kano Teaching Hospital Kano Nigeria. Int Res J Microbiol 2013; 4(9): 226-31.
[26] Farida H, Gasem MH, Suryanto A, et al. Viruses and Gram-negative bacilli dominate the etiology of community-acquired pneumonia in Indonesia, a cohort study. Int J Infect Dis 2015; 38: 101-7.[http://dx.doi.org/10.1016/j.ijid.2015.07.023] [PMID: 26255889]
[27] Taschdjian CL, Kozinn PJ, Toni EF. Opportunistic yeast infections, with special reference to candidiasis. Ann N Y Acad Sci 1970; 174(2): 606-22.[http://dx.doi.org/10.1111/j.1749-6632.1970.tb45586.x] [PMID: 5278139]
[28] Pillary VKG, Wilson DM, Ing TS, Kark RM. Fungus infections in steroid treated SLE. J Am Assoc 1968; 205: 261-5.[http://dx.doi.org/10.1001/jama.1968.03140310019004]
[29] Blaschke S, Don M, Schillinger W, Rüchel R. Candida pneumonia in patients without definitive immunodeficiency. Mycoses 2002; 45(Suppl. 3): 22-6.[http://dx.doi.org/10.1111/j.1439-0507.2002.tb04764.x] [PMID: 12690966]
[30] Abdelaziz S. Antimicrobial resistance pattern of some bacterial pathogens involved in lower respiratory tract infections in Egypt ACTA MICROBIOLOGICA ISSN 2386-7469 2015; 1(1): 22-6.[http://dx.doi.org/10.3823/286]
[31] Onuoha S. Prevalence and antibiotic sensitivity of bacterial agents involved in lower respiratory tract infections. Int J. Biol. Chem. Sci. 2011; 5(2): 774-81.
[32] Bergman M. Association between antimicrobial consumption and resistancein Escherichia coli .antimicrobial agents and chemotherapy, American Society for Microbiology Mar.2009; 912-7.
[33] Salah I. Optimizing antimicrobial drug use in surgery: an intervention strategy in a Sudanese hospital to combat the emergence of bacterial resistant. Elixir Pharmacy 2011; 41: 5657-63.

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"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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