Advance Publication
Tropical Medicine and Health
doi:10.2149/tmh.2013-03
1
Original article
TMHFact-finding
Survey of Nosocomial Infection Control in Hospitals
in Kathmandu, Nepal—A Basis for Improvement
Hiroshi Ohara1*, Bharat M. Pokhrel2, Rajan K. Dahal2, Shyam K. Mishra2, Hari P. Kattel2, Dharma L. Shrestha3,
Yumiko Haneishi1 and Jeevan B. Sherchand2
??
Received 10 January, 2013
Accepted 21 March, 2013
Published online 29 June, 2013
Abstract:
TheSociety
purposeofofTropical
this study
was to investigate the actual conditions of nosocomial infection control in
© 2013
Japanese
Medicine
Kathmandu City, Nepal as a basis for the possible contribution to its improvement. The survey was conducted at
17 hospitals and the methods included a questionnaire, site visits and interviews. Nine hospitals had manuals on
nosocomial infection control, and seven had an infection control committee (ICC). The number of hospitals that
met the required amount of personal protective equipment preparation was as follows: gowns (13), gloves (13),
surgical masks (12). Six hospitals had carried out in-service training over the past one year, but seven hospitals
responded that no staff had been trained. Eight hospitals were conducting surveillance based on the results of bacteriological testing. The major problems included inadequate management of ICC, insufficient training opportunities for hospital staff, and lack of essential equipment. Moreover, increasing bacterial resistance to antibiotics was
recognized as a growing issue. In comparison with the results conducted in 2003 targeting five governmental hospitals, a steady improvement was observed, but further improvements are needed in terms of the provision of high
quality medical care. Particularly, dissemination of appropriate manuals, enhancement of basic techniques, and
strengthening of the infection control system should be given priority.
Key words: Fact finding survey, nosocomial infection control, Kathmandu, Nepal
INTRODUCTION
Recently, nosocomial infections have become a global
concern recognized as a major patient safety issue. They not
only cause a significant burden on patients but also lower
the quality of medical care. In addition, prolonged hospitalization due to nosocomial infections increases costs and unnecessary expenses for the hospital [1, 2]. In the healthcare
setting, particularly in developed countries, various measures including the organization of infection control teams
(ICTs), preparation of manuals, strengthening of surveillance systems, and training of staff have been taken to assure effective control. However, it is only some decades ago
that importance was attached to nosocomial infection control and effective measures were employed, even in developed countries [3].
In developing countries, where the incidence of infectious diseases is high and environmental conditions of
1
healthcare facilities are poor, nosocomial infections may
frequently occur, and some studies have reported a high incidence at healthcare facilities in these countries [4–6]. Effective nosocomial infection control is crucial in the healthcare facilities of developing countries, but in actual fact, attention to it is still limited and control measures are not
functioning well in many facilities. Furthermore, as implementation of control measures seems to be costly and to
consume resources, nosocomial infection control is often
given a low priority.
Severe acute respiratory syndrome (SARS), which
originated in Guangdong Province, China in November
2002, spread to more than 30 countries. In many hospitals
where SARS cases were encountered, nosocomial infections also broke out, causing many casualties along with
economic havoc [7, 8]. It is not overstatement to say that
such outbreaks have heightened awareness regarding nosocomial infection control even in developing countries. In
Bureau of International Medical Cooperation, National Center for Global Health and Medicine, Japan
Department of Microbiology, Institute of Medicine, Tribhuvan University, Nepal
3
Tribhuvan University Teaching Hospital, Institute of Medicine, Nepal
*Corresponding author:
Bureau of International Cooperation, International Medical Center of Japan, 1-21-1, Toyama, Shinjuku-ku, Tokyo 162-8655, Japan
Tel: +81-3-3202-7181
Fax: +81-3-3205-7860
E-mail:
[email protected]
2
2
more recent years, epidemics of novel influenza have also
posed a threat of nosocomial infections [9]. These facts
made many people realize again the importance of strengthening nosocomial infection control at hospitals in developing countries.
Some of the authors of the present paper have been engaged in technical cooperation for nosocomial infection
control with hospitals in developing countries, recognizing
the importance of strengthening control measures in order
to enhance the quality of medical care. Between 2000 and
2009, they have contributed to the promotion of nosocomial
infection control in Vietnam in collaboration with leading
hospitals [10, 11].
Since 2010, in response to the growing concern regarding nosocomial infections, we have focused our efforts in
Nepal through collaboration with Tribhuvan University
Teaching Hospital (TUTH) in Kathmandu City, where a
technical cooperation project by Japan International Cooperation Agency (JICA) had been implemented to strengthen
the hospital. Following studies including those on hospitalacquired diarrheal diseases [12] and the prevalence of multiple drug-resistant pathogens [13], this survey was carried
out as a baseline study aiming to contribute to the improvement of nosocomial infection control at TUTH and consequently in Kathmandu City. The primary purpose of this
study was to evaluate nosocomial infection control conditions and to prepare the basic information needed to provide
technical guidance.
MATERIALS AND METHODS
1. Fact-finding survey of nosocomial infection control
The subjects of this survey are 17 leading hospitals in
Kathmandu City (five national hospitals, nine private hospitals, and three other hospitals). The national hospitals included three general hospitals (one out of three was a university hospital; i.e. TUTH), one pediatric hospital and one
obstetric hospital. All the private hospitals were general
hospitals, while three other hospitals included one semigovernmental hospital and two non-profit organization hospitals (these three hospitals were general hospitals). The 17
hospitals play a crucial role in medical care in Kathmandu
City.
A questionnaire was developed based on the form used
in the previous surveys in Vietnam [11]. The form consisted
of the following items: “general information of the hospitals, control system including manual and infection control
committees (ICC), equipment and facility preparedness,
training conditions, surveillance conditions, expectation for
international cooperation and current problems. The contents of each item in the questionnaire are shown in Table 1.
The questionnaire was distributed to the 17 hospitals in
October 2011 and filled out by the hospital staff members
who were responsible for nosocomial infection control or
the director of the hospital. The recovered data were processed using SPSS Ver19 for Windows. In some hospitals,
to determine the actual situation of ICC, manuals, current
problems and awareness level of hospital staff regarding
nosocomial infection control, direct observations were conducted along with a brief interview with the hospital staff
responsible for nosocomial infection control or hospital di-
Table 1. Questionnare items and contents for 17 hospitals
S.N.
1
2
Questionnare items
General information on hospital
Control system
3
Surveillance conditions
4
Training conditions
5
Equipment and facility prepredness
6
Expectations for assistant partners
7
Current problems
* Training organized by the hospital for the staff
Contents of questionnaire
Type of hospital, number of beds, number of clinical departments
Existence of nosocomial infection control committee, nosocomial infection
control department, infection control team, manual for nosocomial infection
control,
Surveillance according to the report from clinical departments or not,
Bacteriological testing on nosocomial infection cases
Staff who have received training on nosocomial infection control, Hospitals
held in-service training* on nosocomial infection control or not. Hospitals
held in-service training on novel influenza or not, Plan of holding “in-service
training”
Current situation of the preparaton for disinfectants and PPE; Existence of
negative rooms, Isolation rooms in the case of novel influenza/SARS, Plan of
zoning in the hospital according to the risk of infection
Hospital wishes to cooperate with foreign assistant partners or not. What
cooperation does the hospital expect?
Requested the hospital to describe the current problems.
3
rector in addition to the information obtained by the questionnaire.
2. Comparison with the survey results in 2003
In 2003, a questionnaire survey was conducted at five
national hospitals in Kathmandu City [10]. These five hospitals were included in this study (2011). The results of the
2003 questionnaire were compared with those of this study
(2011), including manuals, ICCs, in-service training and
preparedness of personal protective equipment (PPE). A
comparative statistical analysis of the 2003 and 2011 results
was carried out by the Fisher’s exact method using SPSS
Ver19 for Windows.
3. Outline of the technical cooperation project and factfinding survey at TUTH
TUTH was established in 1980 with the assistance of a
grant-aid from the Japanese government as the first medical
school in Nepal, followed by the implementation of a technical cooperation project supported by the JICA from 1980
to 1996 (the corresponding author participated as a team
leader). The purpose of the project was to strengthen medical and educational services at TUTH. During the above period, technical guidance was conducted in the field of hospital management, clinical medicine, nursing management,
laboratory management and medical education. However,
nosocomial infection control was not included in the
project, probably because awareness regarding nosocomial
infection control was still poor in those days even in developed countries including Japan. Currently TUTH is playing
a leading role in medical care as well as human resource development in Nepal as the oldest and one of the most advanced medical schools.
In this study, the current situation of nosocomial infection control at TUTH was investigated in detail as a basis
for further improvement. During the JICA project period,
technical guidance was provided, not on nosocomial infection control, but on bacteriological testing as a priority subject. In this study, investigation was performed by direct observation and interviews with heads of the departments of
clinical microbiology and pharmacology and doctors of internal medicines, focusing on whether bacteriological testing was utilized for implementation of nosocomial infection
control, in addition to detailed observation of the hospital
and the questionnaire survey.
4. Ethical approval
Ethical approval was obtained from the Institute of
Medicine, Kathmandu, Nepal prior to using the questionnaire in the target hospitals.
RESULTS
1. Fact-finding survey of nosocomial infection control
The 17 hospitals responded to most of the questionnaire items, but for some items, a response was obtained
from only 16 hospitals.
General information on hospitals
The average number of beds in the surveyed hospitals
was as follows: national hospitals; 372 (150–497), private
hospitals; 206 (50–750), other hospitals 328 (156–500). The
average number of clinical departments was as follows: national hospitals (excluding the two specialized hospitals);
18.0 (14–22), private hospitals 9.7 (6–15); other hospitals
17.5 (15–20). TUTH, which is one of the national hospitals,
had 468 beds and 22 clinical departments.
Control system
Manuals for infection control were used in 52.9%
(9/17) of the hospitals (national 4/5, private 3/9, and other
hospitals 2/3). However, most of these manuals were more
than five years old and some of their contents were not considered suitable for recent infectious diseases and antibiotic
use. The manuals at three hospitals were considered obsolete. Two national hospitals had good manuals with up-todate contents. Only three hospitals had manuals for novel
influenza.
An infection control committee (ICC) was established
in 41.2% (7/17) of the hospitals (Fig. 1). However, a regular
ICC meeting was held in only two hospitals (once a month,
and every three months) and the remaining hospitals held
meetings when requested. It was noted that the operations
of these committees were far from adequate. No hospitals
had an infection control team (ICT).
Equipment and facility preparedness:
The number of hospitals which met the standard quantity requirements for disinfectants and personal protective
Fig. 1. Hospitals with infection Control Committee (17 hospitals were investigated).
4
equipment (PPE) is shown in Fig. 2. No hospital was
equipped with a sufficient quantity of N95 masks and goggles. Eleven and 12 hospitals responded that N95 masks and
goggles were unavailable, respectively.
A total of 81.3% (13/16) of hospitals responded that
the preparation level for novel influenza was poor or slight.
Four hospitals responded that they could prepare isolation
rooms to deal with novel influenza/ SARS, but no hospital
was equipped with negative pressure rooms. Only one hospital had a plan of zoning formulated according to the risk
of infection.
Training conditions:
Current training conditions are summarized in Table 2.
Six hospitals (four national hospitals, one private hospital
and one other hospital) were organizing training programs
for their staff (in-service training). Regarding future plan,
five hospitals responded that they planned to conduct inservice training, and eight hospitals responded that they did
not have any plans at the present time but hoped to in the future. Among all the hospitals, one had already conducted a
training program on SARS and/or novel influenza and three
hospitals intended to conduct training.
Surveillance conditions:
Bacteriological testing was regularly performed for
nosocomial infection cases at 62.5% (10/16) of the hospitals
and 6.3% (1/16) of the hospitals for some cases. Surveillance of nosocomial infections according to reports from
clinical departments on clinical signs such as fever, respiratory signs, diarrhea, etc. was regularly carried out in 43.8%
(7/16) of the hospitals in the survey (Fig. 3).
Expectation for international cooperation:
Seven hospitals had a strong interest in cooperating
with foreign hospitals. A particularly strong expectation
was observed regarding research support, information supply, PPE provision, and guidance in constructing an effective control system (Table 3).
Current problems:
Among the problems observed in the study were weak
ICC function, few training opportunities among the hospital
staff, inadequate use of antibiotics, shortage of infection
control staff, shortage of doctors and nurses and their overload in daily medical practice, shortage of fundamental
equipment including PPE, inadequate practice of basic tech-
Fig. 2. Hospitals satisfying standard requirements for personal
protective equipment (PPE) and disinfectants (17 hospitals were investigated).
Fig. 3. Surveillance conditions (17 hospitals were investigated).
Table 3. Expectations for international cooperation
Table 2. Training activities
Training
Hospital staff received
training for nosocomial
Infection control
Hospital held in-service
training for nosocomial
infection control
Hospital held in-service
training on novel influenza
No. hospital
None
7
A small number
7
Majority of staff
2
No
10
Yes
6
No
15
Yes
1
Training: training programs including those organized by other
hospitals and the hospital that the staff belong to.
In-service training: training programs organized by the hospital
to which the staff belong (16 hospitals were investigated)
S.N.
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
No. of
Hospitals
Support in research
7
Information provision
6
Supply of personal protective equipment
5
Improvement in the nosocomial infection control
4
system
Supply of ICU and emergency equipment
4
Guidance in accepting patients
3
Training for the staff
3
Supply of disinfectants
3
Supply of laboratory equipment
2
Renovation of hospital facilities
2
Description
5
Performance of bacteriological testing was well carried out in the clinical microbiology department of TUTH,
and the results were passed on to the clinical side through
the drug information office. However, the interview suggested that increased bacterial resistance to antibiotics was
a growing issue at TUTH.
DISCUSSION
Fig. 4. Comparison of infection control conditions between
2003 and 2011.
* Hospitals with sufficient or nearly sufficient amounts
of PPE, disinfectants based on Ministry of Health
standards; five national hospitals were investigated.
niques such as standard precautions, inappropriate use of
surveillance results, improper disinfection and sterilization
methods, and low awareness regarding nosocomial infection control.
2. Comparison of 2003 and 2011 survey results
Comparison of nosocomial infection control conditions between 2003 and 2011 at five national hospitals
showed an improvement trend. Particularly, preparation of
PPE and disinfectants remarkably improved as shown in
Figure 4 (P = 0.0238 and P = 0.004, respectively), categories in which all five hospitals met the standard quantity. In
2011, four out of five hospitals (except for one specialized
hospital) were conducting in-service training, while only
one hospital was conducting such training in 2003 (P =
0.099). Among these four hospitals, manuals were on hand
and an ICC was established (P = 0.4167).
3. Nosocomial infection control situation at TUTH
The first ICC in Nepal was established in 1988 at
TUTH. Since then, an ICC meeting has been held once a
month. A comparatively good infection control manual was
prepared and has been revised according to necessity. Inservice training has been conducted for most of the staff at
TUTH. This study showed a good situation regarding
equipment preparedness including disinfectant (sufficient
amount), PPE (sufficient amount of ordinary masks, disposable gloves and gowns) along with preparation of isolation
rooms. However, incomplete observance of basic techniques such as standard precautions, as well as the need to
further strengthen the function of ICC, have been pointed
out as challenges.
Appropriate nosocomial infection control is a key
strategy in providing high quality medical care, and effective measures are particularly required in developing countries, where the frequency of infectious diseases is high and
environmental conditions of hospitals are poor [14, 15].
However, nosocomial infection control is generally not
given high priority, and awareness among medical practitioners is still low, a situation that jeopardizes health care functions.
In this survey in Kathmandu City, steady progress was
observed in national hospitals in comparison with the results in 2003. It is particularly noteworthy that awareness
among staff and the level of training activities increased
with an improvement in the preparedness of essential infection control equipment such as PPE and disinfectants. Regarding private hospitals and other hospitals, a comparative
study was not conducted using this survey, but an improvement in infection control similar to that of the national hospitals is assumed.
However, further efforts to strengthen nosocomial infection control at the target hospitals are still considered
necessary. The results showed that the majority of hospitals
did not have an up-to-date nosocomial infection control
manual, that the surveillance system was not established
sufficiently, and that preparations against SARS and novel
influenza were poor. It is crucial to improve these fundamental systems. Moreover, special emphasis should be
placed on observance of basic techniques (standard precautions) such as hand hygiene, effective use of PPE and appropriate practice of disinfection [16–18]. Enlightenment activities, such as distribution of manuals and teaching materials and the organization of training courses for medical
staff, are very useful and effective for the improvement of
nosocomial infection control. An increasing number of hospitals have been establishing ICCs in recent years, but the
management and implementation of activities need further
improvement to achieve effective control measures. Hereafter, ICTs also need to be set up in leading hospitals. Furthermore, the detailed status of nosocomial infections and their
causative agents should be strictly monitored and properly
utilized in clinical practice.
Among the targeted hospitals in this survey, TUTH
6
showed comparatively good results. Bacteriological testing,
supervised by the JICA project, was functioning well and
contributing to the surveillance of nosocomial infection
based on bacteriological examination and reports from clinical departments for suspected nosocomial infection cases.
However, our previous study on pathogens associated with
nosocomial lower respiratory infections showed a high
frequency of gram negative bacilli such as Escherichia coli,
Pseudomonas aerginosa, Acinetobactor baumanii,
Klebsiella pneumoniae, as well as a high multiple drug resistance rate for isolated bacteria. In addition, a high rate of
extended stratum beta lactamase (ESBL) producing bacteria
was observed [13]. The spread of multi-resistant bacteria reported by many developing countries is considered to be a
facilitating factor in nosocomial infection [19–21]. Methallo β lactamase (MBL) producing bacteria, which originated from India, is also suspected to be spreading to Nepal
[13, 22]. These findings suggest the need for more aggressive measures to tackle this global threat. The appropriate
use of antibiotics based on accurate bacteriological testing,
along with appropriate guidelines, is a worldwide challenge.
Nepal, fortunately, has not experienced a SARS outbreak, and no human case of avian influenza has been reported to date. On the other hand, awareness of nosocomial
infection control seems to be lagging behind countries
where a SARS outbreak did occur as shown in the 2003
study [10]. When a novel influenza becomes an epidemic
and human to human infection is common, nosocomial infections may easily occur as seen in the Spanish influenza
pandemic of 1918–1919. Appropriate nosocomial infection
control is also considered useful for novel influenza control.
Special importance should be placed on setting up a foundation for appropriate nosocomial infection control in daily
practice, training medical staff and establishing a control
system, before nosocomial infections become a frequent occurrence.
Nosocomial infection control is crucial in providing
high quality medical care. Greater efforts should be focused
on training medical staff to enhance basic techniques and
establish control systems at ordinary times, not waiting until
after an outbreak or epidemic. With such a foundation, it
will be possible to promptly apply stringent nosocomial infection control in the event of an outbreak of novel influenza, SARS or other emerging infectious disease. These
measures will contribute to the reduction of unnecessary
costs and can improve the financial condition of the hospital.
Based on the results of this survey, the authors intend
to collaborate with Nepalese authorities and further contribute to the improvement of nosocomial infection control.
Currently, our collaborative activities at TUTH are related
to basic studies on bacterial resistance to antibiotics and the
appropriate use of antibiotics. In addition, guidance on the
promotion of standard precautions and surveillance systems
is currently being prepared. The results of the present survey are expected to provide baseline data for monitoring the
progress of the nosocomial infection control situation at
TUTH as well as that in hospitals in Kathmandu.
In this survey, only hospitals in Kathmandu City were
investigated. Infection control conditions are improving in
these hospitals but further improvement in the software aspect is still needed to assure high quality medical care. In
Nepal as well as other developing countries, a significant
disparity in the conditions of medical care and the health
system exists between major cities and rural areas. In the future, the expansion of nosocomial infection control to hospitals in remote areas will be needed along with the implementation of guidance for hospitals in those areas.
ACKNOWLEDGEMENTS
The authors would like to express thanks to the 17 hospitals in Kathmandu City for their cooperation during the
implementation of this study. This survey was conducted
with the support of grants from the National Center for
Global Health and Medicine, Japan.
CONFLICT OF INTEREST
None.
REFERENCES
1. Vrijens F, Hulstaert F, Devriese S, van de Sande S.
Hospital-acquired infections in Belgian acute-care hospital: an estimation of their global impact on mortality,
length of stay and healthcare costs. Epidemiol Infect 2012;
140: 126–136.
2. Wilcox MH, Dave J. The cost of hospital-acquired infection and the value of infection control. J Hosp Infect 2000;
45: 81–84.
3. Harbarth S. What can we learn from each other in infection
control? Experience in Europe compare with the USA. J
Hosp Infect 2013; 83: 173–184.
4. Rosenthal VD. Health-care-associated infections in developing countries. Lancet 2011; 377: 186–188.
5. Wolkewitz M, Di Termini S, Cooper B, Meerpohl J,
Schumacher M. Paediatric hospital-acquired bacteraemia
in developing countries. Lancet 2012; 379: 1484.
6. Aiken AM, Wanyoro AK, Mwangi J, Mulingwa P,
Wanjohi J, Njoroge J, Juma F, Mugoya IK, Scott JAG,
Hall AJ. Evaluation of surveillance for surgical site infections in Thika Hospital, Kenya. J Hosp Infect 2013; 83:
7
140–145.
7. Poutanen SM, Low DE, Henry B, Finkelstein S, Rose D,
Green K, Tellier R, Draker R, Adachi D, Ayers M, Chan
AK, Skowronski DM, Salit I, Simor AE, Slutsky AS,
Doyle PW, Krajden M, Petric M, Brunham RC, McGeer
AJ; National Microbiology Laboratory, Canada; Canadian
Severe Acute Respiratory Syndrome Study Team. Identification of severe acute respiratory sundrome in Canada.
New Engl J Med 2003; 348: 1995–2005.
8. Ohara H. Experience and review of SARS control in
Vietnam and China. Trop Med Health 2004; 32: 235–240.
9. Cheng VC, Tai JW, Wong LM, Chan JF, Li IW, To KK,
Hung IF, Chan KH, Ho PL, Yuen KY. Prevention of nosocomial transmission of swine-origin pandemic influenza
virus A/H1N1 by infection control bundle. J Hosp Infect
2010; 74: 271–277.
10. Ohara H, Nguyen VH, Truong AT, Tran Q. Report on
Japan-Vietnam collaboration in nosocomial infection control in Bach Mai Hospital, Hanoi from 2000 to 2006. Trop
Med Health 2007; 35: 253–259.
11. Ohara H, Hung NV, Truong AT. Fact-finding survey of
nosocomial infection control in hospitals in Vietnam and
application to training programs. J Infect Chemother 2009;
15: 384–389.
12. Sherchan JB, Ohara H, Sherchand JB, Tandukar S,
Sakurada S, Gurung B, Ansari S, Rijal BP, Pokhrel BM.
Molecular evidence based hospital acquired rotavirus gastroenteritis in Nepal. Prime J Microbiol Research 2011; 1:
16–21.
13. Shrestha S, Chaudhari R, Karmacharya S, Kattel HP,
Mishra SK, Dahal RK, Bam N, Banjade N, Rijal BP,
Sherchand JB, Ohara H, Koirara J, Pokhrel BM. Prevalence of nsocomial lower respiratory tract infections
caused by multi drug resistance pathogens. J Inst Med
2011; 33: 7–14.
14. Hughes AJ, Ariffin N, Huat TL, Abdul Molok H, Hashim
15.
16.
17.
18.
19.
20.
21.
22.
S, Sarijo J, Abd Latif NH, Abu Hanifah Y, Kamarulzaman
A. Prevalence of nosocomial infection and antibiotic use at
a university medical center in Malaysia. Infect Control
Hosp Epidemiol 2005; 26: 100–104.
Gill CJ, Mantaring JBV, Macleod WB, Mendoza M,
Mendoza S, Huskin WC, Goldmann DA, Hamer DH. Impact of enhanced infection control at two neonatal intensive care units in the Philippines. Clin Infect Dis 2009; 48:
13–21.
Apisarnthanarak A, Fraser VJ. Feasiblility and efficacy of
infection control interventions to reduce the number of
nosocomial infections and drug-resistant microorganisms
in developing countries: What else do we need?. Clin
Infect Dis 2009; 48: 22–24.
Alp E, Ozturk A, Guven M, Celik I, Doganay M, Voss A.
Importance of structured training programs and good role
models in hand hygiene in developing countries. J Infect
Public Health 2011; 4: 80–90.
Stewardson AJ, Allegranzi B, Perneger TV, Attar H, Pittet
D. Testing the WHO hand hygiene self-assessment framework for usability and reliability. J Hosp Infect 2013; 83:
30–35.
Falagas ME, Karveli EA, Siempos II, Vardakas KZ. Acinetobacter infections: a growing threat for critically ill patients. Epidemiol Infect 2008; 136: 1009–1019.
Heritier C, Poirel L, Lambert T, Nordmann P. Contribution
of acquired carbapenem-hydrolyzing oxacillinase to carbapenem resistance in Acinetobacter baumannii. J
Antimicrob Agents Chemother 2005; 49: 3198–3202.
Subha A, Ananthan S. Extended spectrum beta-lactamase
(ESBL) medicated resistance to third generation cephalosporins among Klebsiella pneumonia in Chhenai. Indian
J Med Microbiol 2002; 20: 92–95.
Rolain JM, Parola P, Cornaglia G. New Delhi MetalloBeta-Lactamase (NDM-1): towards a new pandemia? Clin
Microbiol Infect 2010; 16: 1699–1701.