The Open Respiratory Medicine Journal




ISSN: 1874-3064 ― Volume 13, 2019
RESEARCH ARTICLE

Prevalence and Risk Factors for Latent Tuberculosis Infection among Healthcare Workers in a Low Incidence Country



Luca Coppeta*, Antonio Pietroiusti, Anna Neri, Aurelio Janni, Savino Baldi, Francesca Papa, Andrea Magrini
Occupational Medicine Department, University of Rome “Tor Vergata”, Viale Oxford 81, 00133 Roma, Italy

Abstract

Background:

Tuberculosis prevention is a major goal in the hospital setting. Because of the possible progression or reactivation of latent disease, the screening of healthcare workers is an important issue in the TB control program. The aim of the study was to assess the prevalence of LTBI (latent tuberculosis infection) and to evaluate the main risk factors related to this condition in a teaching hospital in Italy.

Methods:

We reviewed the data of a tuberculosis screening conducted on 3622 healthcare professionals in a teaching hospital in Rome. All subjects were evaluated by QuantiFERON test which if positive, was followed by appropriate clinical and diagnostic procedures.

Results:

Latent Tuberculosis Infection LTBI condition was detected in 2.1% of the cases, most commonly in men. Male gender, higher age class, country of birth and nurse job were statistically related with the positivity to QuantiFERON test.

Conclusion:

LTBI was relatively uncommon in our population, however, given the potential risk of reactivation and progression to overt disease, the screening of healthcare workers and students is recommended in the hospital of low-incidence countries.

Keywords: Latent tuberculosis, Contact screening, QuantiFERON, Occupational health, Bacillus, Mycobacterium.


Article Information


Identifiers and Pagination:

Year: 2019
Volume: 13
First Page: 1
Last Page: 4
Publisher Id: TORMJ-13-1
DOI: 10.2174/1874306401913010001

Article History:

Received Date: 16/01/2019
Revision Received Date: 30/03/2019
Acceptance Date: 08/04/2019
Electronic publication date: 30/04/2019
Collection year: 2019

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© 2019 Coppeta 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 Occupational medicine department, University of Rome “Tor Vergata”, Viale Oxford 81, 00133 Roma, Italy; Tel: +39 3471080262, Email: lcoppeta@gmail.com




1. INTRODUCTION

Tuberculosis (TB) is a major public health problem that bears many occupational consequences [1CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141.].

130 years after the discovery of the tubercle Bacillus, the prevalence of infection remains high. It has been estimated that approximately one-third of the world's population carries tubercular Mycobacterium in a latency State, which accounts for over 2 billion people [2Ministero del Lavoro della Salute e delle Politiche Sociali. Aggiornamento delle raccomandazioni per le attività di controllo della tubercolosi in Italia 2013.http://www.salute.gov.it/imgs/C_17_ pubblicazioni_1221_allegato.pdf]. There are 8.6 million new cases per year and nearly 2 million deaths/year, 30% of which are preventable with the appropriate treatment.

With TB incidence rate being considerably below 10 cases per 100,000 inhabitants over the last 10 years, Italy [3Istituto Superiore di Sanità. Tubercolosi Aspetti epidemiologici: dati generali http://www.epicentro.iss.it/problemi/Tubercolosi/epid.asp] is characterized by a low incidence in the general population, with a concentration of most cases in some risk groups and in some age groups. In the decade between 2004 and 2014, an average of 4300 cases of tuberculosis were notified annually, 52% of which were in foreigners.

Despite being preventable and treatable, tuberculosis is still one of the most dramatic health emergencies, and it was declared as a global emergency in 1993 by the WHO due to the health, economic and social burden that it bears.

Known risk factors for tuberculosis infection include living in overcrowded communities, immigration from endemic areas and individual conditions such as malnutrition, alcoholism, diabetes, drug addiction, HIV infection, age [1CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141.].

Healthcare workers (HCWs) are at higher risk of being exposed to tuberculosis compared to the general population [1CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141.], even in countries with low TB incidence, such as Italy. In these workers, the assessment of latent (LTBI) and active (TBA) tuberculosis is part of the annual health surveillance program aimed to prevent occupational diseases [2Ministero del Lavoro della Salute e delle Politiche Sociali. Aggiornamento delle raccomandazioni per le attività di controllo della tubercolosi in Italia 2013.http://www.salute.gov.it/imgs/C_17_ pubblicazioni_1221_allegato.pdf].

Because of the severity of their symptoms, individuals with an active contagious form of tuberculosis have a higher chance of being hospitalized and can remain for hours or days at the health care facility with a pending diagnosis. For these reasons, the prevention of nosocomial transmission of tuberculosis represents prominent public health and occupational requirement [4National Tuberculosis Controllers Association; Centers for Disease Control and Prevention (CDC). Guidelines for the investigation of contacts of persons with infectious tuberculosis. Recommendations from the National Tuberculosis Controllers Association and CDC. MMWR Recomm Rep 2005; 54(RR-15): 1-47.[PMID: 16357823] , 5 Ministero del Lavoro della Salute e delle Politiche Sociali. Prevenzione della tubercolosi negli operatori sanitari e soggetti ad essi equiparati. Approvato come Accordo nella Conferenza Stato-Regioni-Province Autonome del 7 febbraio 2013]. However, it is also important to note that healthcare providers may contract an infectious disease outside of the workplace, thus representing a source of infection to colleagues and patients that are more likely to be affected.

A case of untreated active infectious pulmonary tuberculosis can infect 10-15 people within a year [6WHO. WHO policy on TB infection control in health-care facilities, congregate settings and households http://whqlibdoc.who.int/ publications/2009/9789241598323_eng.pdf]. Of these individuals, a percentage between 3 and 10% will be infected, half of whom will become ill within one to two years while the others might develop the illness at any point of their residual life [4National Tuberculosis Controllers Association; Centers for Disease Control and Prevention (CDC). Guidelines for the investigation of contacts of persons with infectious tuberculosis. Recommendations from the National Tuberculosis Controllers Association and CDC. MMWR Recomm Rep 2005; 54(RR-15): 1-47.[PMID: 16357823] ]. On average, 10% of people with LTBI develop TB disease in their lifetime, half of which become ill within 2 years after exposure [1CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141.]. About 70% of incident cases of TB are a result of the reactivation of a past infection [1CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141., 4National Tuberculosis Controllers Association; Centers for Disease Control and Prevention (CDC). Guidelines for the investigation of contacts of persons with infectious tuberculosis. Recommendations from the National Tuberculosis Controllers Association and CDC. MMWR Recomm Rep 2005; 54(RR-15): 1-47.[PMID: 16357823] , 6WHO. WHO policy on TB infection control in health-care facilities, congregate settings and households http://whqlibdoc.who.int/ publications/2009/9789241598323_eng.pdf]. For these reasons, the identification and prophylactic treatment of individuals with LTBI are crucial for the elimination of the disease.

According to Italian law [7 Decreto legislativo 9 aprile 2008, n. 81 “Attuazione dell’articolo 1 della legge 3 agosto 2007, n. 123, in materia di tutela della salute e della sicurezza nei luoghi di lavoro”., 8 Conferenza permanente per i rapporti tra lo Stato, le Regioni e le Province Autonome di Trento e Bolzano – Provvedimento 17 dicembre 1998 – Linee Guida per il controllo della malattia tubercolare, su proposta del Ministro della Sanità, ai sensi dell’art. 115, comma 1, lettera b), del decreto legislativo 31 marzo 1998, n. 112.], it is mandatory for employers to evaluate all risks in the workplace, including the risk of exposure to biological agents, and to implement measures to prevent the spread to operators or to limit the severity of its consequences. For this purpose, great importance is given to health surveillance of tuberculosis infection. In fact, the surveillance of LTBI in HCWs is considered fundamental for tuberculosis prevention.

The aim of our study was to estimate LTBI prevalence and evaluate associated risk-factors among Italian HCWs

2. METHODS

LTBI is defined as a state of a persistent immune response to stimulation by Mycobacterium tuberculosis antigens without evidence of clinically manifested active TB. The prevalence of the LTBI was retrospectively evaluated by analyzing the results of the QuantiFERON-TB Gold (QFT) tests performed in the HCWs of a teaching hospital in Rome. The health workers in the study were evaluated during the annual health surveillance program performed in 2015.

The tests results were classified according to the interpretative guidelines provided by the manufacturer. Tests were classified as “positive” or “negative”, respectively, if higher or lower response than the cut-off value of 0.35 IU / ml of INF-γ was detected in at least one test tube (TB1 or TB2). All the workers with a “positive” result had to perform diagnostic tests to exclude active tuberculosis such as chest X-ray, and blood chemistry. The final medical evaluation was done by a specialist in infectious diseases. A subject was diagnosed as affected by LTBI in the case of positivity to the QFT-Plustest in the absence of clinical-radiological and serological signs of active infection.

The analyzed sample included medical doctors, nurses, lab and radiology technicians and medical students. Positive LTBI workers were assessed again within a year since the first positive serological result. We also analyzed the phenomenon of reversion which was defined as the possible reversal of QFT-Plus test positivity in the year after the revealing of positivity (2016).

Data were analyzed using the statistical software IBM SPSS. A p-value of 0.05 was taken as the level of statistical significance. The inference of the analyzed factors was expressed as OR and respective 95% Confidence Intervals (95% C.I.) and p-value.

3. RESULTS

3622 clinical records were examined (1295 men and 2327 women); the average age of the population was 32.2 ± 10.5 years in males and 33.5 ± 11.1 years in women, respectively. LTBI was diagnosed in 77 subjects (2.1% of the sample). The mean age of the subjects with LTBI was 42.9 ± 12.8 years vs 31.8 ± 10.5 for the subjects that tested negative; (p 0.001 at T-test). The prevalence of LTBI in relation to mail demographic and occupational factors of the studied population is shown in Table 1. Male gender, age 40 years, foreign country of birth and nurse job was related to the risk of LTBI after testing those factors in a multivariate analysis (Table 2).

Table 1
Prevalence of LTBI in the working population per gender, age group, country of birth and occupation.


Table 2
Risk factors for LTBI in the study population (multivariate analysis).


The reversion phenomenon (defined by the negativization of a positive test) was documented in 2 subjects (2.6% of the positive cases). LTBI subjects in relation to the date of first positive feedback and reversal of the test were classified as shown in Table 3.

Table 3
The number of subjects with LTBI per gender and time of onset.


Conversion rate among our population was 0.5% (9 confirmed positive test among 1455 subjects who had previous negative determination in the year 2014).

Among the subjects classified as having LTBI, most consisted of nurses (36/77: 46,8 percent), while medical students (17/79; 22,0%), physicians (14/77; 18.2%), and technicians (10/77; 13,0%) were less represented. For 59 subjects, chemoprophylaxis was prescribed by infectious disease specialist. Eighteen subjects refused therapy while 9 did not return to visit after the prescription. No case of active TB has been documented between subjects LTBI positive in the year following the study.

4. DISCUSSION

The QuantiFERON test is confirmed to be a useful diagnostic tool, that is easy to perform on groups of exposed workers. It has been sufficiently validated in clinical use and comes with a good positive predictive value. The results of our study confirm the low prevalence of the LTBI condition among the Italian population. When compared with data from studies carried out among hospital population, our work shows a lower prevalence of LTBI condition (2.6% versus mean LTBI percentages of 9.2% found in other studies) [9Zwerling A, van den Hof S, Scholten J, Cobelens F, Menzies D, Pai M. Interferon-gamma release assays for tuberculosis screening of healthcare workers: A systematic review. Thorax 2012; 67(1): 62-70.[http://dx.doi.org/10.1136/thx.2010.143180] [PMID: 21228420] -12Schablon A, Beckmann G, Harling M, Diel R, Nienhaus A. Prevalence of latent tuberculosis infection among health care workers in a hospital for pulmonary diseases. J Occup Med Toxicol 2009; 4: 1.[http://dx.doi.org/10.1186/1745-6673-4-1] [PMID: 19134168] ]. This difference is reasonably related to the low average age of the sample, which equates to a shorter period of exposure.

Moreover, the lower prevalence of LTBI found in our population can be related to the effectiveness of the administrative and environmental control plan carried out in our hospital since 2005, that provides for early reporting of suspected or confirmed case of TB. In previous studies conducted in our hospital [15Magrini A, Coppeta L, Somma G, et al. Risk of tuberculosis in healthcare workers: Risk assessment and medical surveillance. Ig Sanita Pubbl 2016; 72(2): 137-43.[PMID: 27336958] ] during the period 2007/2013, the mean prevalence of positive tests was 5.5%.

A small retrospective study conducted by Lamberti et al. in 2016 [11Lamberti M, Muoio MR, Westermann C, Nienhaus A, Arnese A. RibeiroSobrinho AP, Di Giuseppe G, Garzillo EM, Crispino V, Coppola N, De Rosa A. Prevalence and associated risk factors of latent tuberculosis infection among undergraduate and postgraduate dental students: A retrospective study. Arch Environ Occup Health 2016; 1-7. [Epub ahead of print].] on a population of dentistry students showed a prevalence of 2.84% for LTBI, which is in line with what was found in our study. The same authors in previous studies of larger populations showed a prevalence of 1.29%.

After testing in a multivariate analysis, LTBI condition was statistically related to the male gender, age 40years, and birth in a foreign state (out of Italy); moreover, nurses work, in our study, seems to be associated with a higher prevalence of LTBI as reported in the literature [12Schablon A, Beckmann G, Harling M, Diel R, Nienhaus A. Prevalence of latent tuberculosis infection among health care workers in a hospital for pulmonary diseases. J Occup Med Toxicol 2009; 4: 1.[http://dx.doi.org/10.1186/1745-6673-4-1] [PMID: 19134168] ]. The phenomenon of reversion, defined as the reversal of QFT-Plus test positivity in the year after the revealing of positivity and widely described in the literature [13Banaei N, Gaur RL, Pai M. M. PaiInterferon γ release assays for latent tuberculosis: What are the sources of variability? J Clin Microbiol 2016; 54(4): 845-50.[http://dx.doi.org/10.1128/JCM.02803-15] [PMID: 26763969] -15Magrini A, Coppeta L, Somma G, et al. Risk of tuberculosis in healthcare workers: Risk assessment and medical surveillance. Ig Sanita Pubbl 2016; 72(2): 137-43.[PMID: 27336958] ], manifested in 2.5% of positive results. This phenomenon appeared to be common in subjects with lower values of IFN production at QuantiFERON test.

In a previous evaluation relative to the year 2014 we found a 16% reversion rate, much higher than the actual. Actions taken in our hospital to implement standardization of procedures for specimen collection, storage and transport of samples during the study year, may justify the lower incidence of the phenomenon than in previous statistics. It is also known that reversion may be indicative of transient infections that can occur when someone is exposed to infectious cases of active tuberculosis [16Verrall AJ, Netea MG, Alisjahbana B, Hill PC, van Crevel R. Early clearance of Mycobacterium tuberculosis: A new frontier in prevention. Immunology 2014; 141(4): 506-13.[http://dx.doi.org/10.1111/imm.12223] [PMID: 24754048] , 17Nardell EA, Wallis RS. Here today gone tomorrow: The case for transient acute tuberculosis infection. Am J Respir Crit Care Med 2006; 174(7): 734-5.[http://dx.doi.org/10.1164/rccm.200607-923ED] [PMID: 16988164] ]; a more timely identification and management of cases may have had, therefore, an impact in lowering this phenomenon.

A large number of positive cases (17/79; 22,0%) were reported among medical students who nevertheless constituted the largest population in our sample. Although these subjects need to be included in programs for the prevention of infection and diagnosis of latent tuberculosis infection, they are not usually considered a possible source of risk for operators and patients. Despite the frequency of LTBI in these subjects is reported to be very low [18Durando P, Sotgiu G, Spigno F, et al. Latent tuberculosis infection and associated risk factors among undergraduate healthcare students in Italy: A cross-sectional study. BMC Infect Dis 2013; 13: 443.[http://dx.doi.org/10.1186/1471-2334-13-443] [PMID: 24059355] , 19Durando P, Alicino C, Orsi A, et al. Latent tuberculosis infection among a large cohort of medical students at a teaching hospital in Italy. BioMed Res Int 2015; 2015746895[http://dx.doi.org/10.1155/2015/746895] [PMID: 25705685] ], the results of our study confirm the need to extend the evaluation of LTBI to this population.

Given the rate of progression and reactivation reported in the literature [1CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141., 3Istituto Superiore di Sanità. Tubercolosi Aspetti epidemiologici: dati generali http://www.epicentro.iss.it/problemi/Tubercolosi/epid.asp], we can estimate that among the individuals of our study affected by LTBI, 2 to 4 workers will develop active tuberculosis throughout working life.

Regarding the suitability for the job, according to the main scientific statements [1CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141., 4National Tuberculosis Controllers Association; Centers for Disease Control and Prevention (CDC). Guidelines for the investigation of contacts of persons with infectious tuberculosis. Recommendations from the National Tuberculosis Controllers Association and CDC. MMWR Recomm Rep 2005; 54(RR-15): 1-47.[PMID: 16357823] , 6WHO. WHO policy on TB infection control in health-care facilities, congregate settings and households http://whqlibdoc.who.int/ publications/2009/9789241598323_eng.pdf], preventative therapy should be offered to those who don’t have contraindications. Workers who refuse to submit to this therapy will not be automatically excluded from their occupation. However, an occupational medicine specialist will evaluate whether transferring them in a ward with a lower risk for operator-patient contagion. In the first 2 years following the diagnosis, health surveillance must be performed every six months at most. Subjects with a reversion of a positive test or conversion-reversion phenomenon need to be re-evaluated by occupational medicine specialist according to the risk evaluation.

CONCLUSION

The results of our study confirm the low prevalence of LTBI in the Italian healthcare workers. Despite this, the condition of LTBI is not contagious and the different circumstances of diagnosis require specific clinical and preventive considerations.

AUTHORS' CONTRIBUTIONS

LC contributed to study design and interpretation of results and was the major contributor in writing the paper; AN and AJ interpreted data results and was a contributor in writing the paper; FP collected references and participated in statistical analysis; AP interpreted data results; AM contributed to study design and interpreted data results.

LIST OF ABBREVIATIONS

LTBI = Latent Tuberculosis Infection
TB = Tuberculosis
HCWs = Healthcare Workers
TBA = To Be Announced
QFT = QuantiFERON-TB
CI = Confidence Intervals

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

All procedures performed in this study were approved by the ethical committee of Policlinic Tor Vergata.

HUMAN AND ANIMAL RIGHTS

No animals/humans were used for studies that are the basis of this research.

CONSENT FOR PUBLICATION

Written consent was obtained from all participants.

AVAILABILITY OF DATA AND MATERIALS

The data sets used and/or analyzed during the current study are available from the corresponding author.

FUNDING

None.

CONFLICT OF INTEREST

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

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

[1] CDC Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health - Care Settings MMWR 2005; 54(No. RR-17): 1-141.
[2] Ministero del Lavoro della Salute e delle Politiche Sociali. Aggiornamento delle raccomandazioni per le attività di controllo della tubercolosi in Italia 2013.http://www.salute.gov.it/imgs/C_17_ pubblicazioni_1221_allegato.pdf
[3] Istituto Superiore di Sanità. Tubercolosi Aspetti epidemiologici: dati generali http://www.epicentro.iss.it/problemi/Tubercolosi/epid.asp
[4] National Tuberculosis Controllers Association; Centers for Disease Control and Prevention (CDC). Guidelines for the investigation of contacts of persons with infectious tuberculosis. Recommendations from the National Tuberculosis Controllers Association and CDC. MMWR Recomm Rep 2005; 54(RR-15): 1-47.[PMID: 16357823]
[5] Ministero del Lavoro della Salute e delle Politiche Sociali. Prevenzione della tubercolosi negli operatori sanitari e soggetti ad essi equiparati. Approvato come Accordo nella Conferenza Stato-Regioni-Province Autonome del 7 febbraio 2013
[6] WHO. WHO policy on TB infection control in health-care facilities, congregate settings and households http://whqlibdoc.who.int/ publications/2009/9789241598323_eng.pdf
[7] Decreto legislativo 9 aprile 2008, n. 81 “Attuazione dell’articolo 1 della legge 3 agosto 2007, n. 123, in materia di tutela della salute e della sicurezza nei luoghi di lavoro”.
[8] Conferenza permanente per i rapporti tra lo Stato, le Regioni e le Province Autonome di Trento e Bolzano – Provvedimento 17 dicembre 1998 – Linee Guida per il controllo della malattia tubercolare, su proposta del Ministro della Sanità, ai sensi dell’art. 115, comma 1, lettera b), del decreto legislativo 31 marzo 1998, n. 112.
[9] Zwerling A, van den Hof S, Scholten J, Cobelens F, Menzies D, Pai M. Interferon-gamma release assays for tuberculosis screening of healthcare workers: A systematic review. Thorax 2012; 67(1): 62-70.[http://dx.doi.org/10.1136/thx.2010.143180] [PMID: 21228420]
[10] Uden L, Barber E, Ford N, Cooke GS. Risk of tuberculosis infection and disease for health care workers: An updated meta-analysis. Open Forum Infect Dis 2017; 4(3): ofx137.
[11] Lamberti M, Muoio MR, Westermann C, Nienhaus A, Arnese A. RibeiroSobrinho AP, Di Giuseppe G, Garzillo EM, Crispino V, Coppola N, De Rosa A. Prevalence and associated risk factors of latent tuberculosis infection among undergraduate and postgraduate dental students: A retrospective study. Arch Environ Occup Health 2016; 1-7. [Epub ahead of print].
[12] Schablon A, Beckmann G, Harling M, Diel R, Nienhaus A. Prevalence of latent tuberculosis infection among health care workers in a hospital for pulmonary diseases. J Occup Med Toxicol 2009; 4: 1.[http://dx.doi.org/10.1186/1745-6673-4-1] [PMID: 19134168]
[13] Banaei N, Gaur RL, Pai M. M. PaiInterferon γ release assays for latent tuberculosis: What are the sources of variability? J Clin Microbiol 2016; 54(4): 845-50.[http://dx.doi.org/10.1128/JCM.02803-15] [PMID: 26763969]
[14] Schablon A, Nienhaus A, Ringshausen FC, Preisser AM, Peters C. Occupational screening for tuberculosis and the use of a borderline zone for interpretation of the IGRA in German healthcare workers. PLoS One 2014; 9(12)e115322[http://dx.doi.org/10.1371/journal.pone.0115322] [PMID: 25541947]
[15] Magrini A, Coppeta L, Somma G, et al. Risk of tuberculosis in healthcare workers: Risk assessment and medical surveillance. Ig Sanita Pubbl 2016; 72(2): 137-43.[PMID: 27336958]
[16] Verrall AJ, Netea MG, Alisjahbana B, Hill PC, van Crevel R. Early clearance of Mycobacterium tuberculosis: A new frontier in prevention. Immunology 2014; 141(4): 506-13.[http://dx.doi.org/10.1111/imm.12223] [PMID: 24754048]
[17] Nardell EA, Wallis RS. Here today gone tomorrow: The case for transient acute tuberculosis infection. Am J Respir Crit Care Med 2006; 174(7): 734-5.[http://dx.doi.org/10.1164/rccm.200607-923ED] [PMID: 16988164]
[18] Durando P, Sotgiu G, Spigno F, et al. Latent tuberculosis infection and associated risk factors among undergraduate healthcare students in Italy: A cross-sectional study. BMC Infect Dis 2013; 13: 443.[http://dx.doi.org/10.1186/1471-2334-13-443] [PMID: 24059355]
[19] Durando P, Alicino C, Orsi A, et al. Latent tuberculosis infection among a large cohort of medical students at a teaching hospital in Italy. BioMed Res Int 2015; 2015746895[http://dx.doi.org/10.1155/2015/746895] [PMID: 25705685]

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