Human Vaccines & Immunotherapeutics
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Implication of health care personnel in measles transmission Núria Torner, Ruben Solano, Cristina Rius, Angela Domínguez & the Measles Elimination Program Surveillance Network of Catalonia, Spain To cite this article: Núria Torner, Ruben Solano, Cristina Rius, Angela Domínguez & the Measles Elimination Program Surveillance Network of Catalonia, Spain (2015) Implication of health care personnel in measles transmission, Human Vaccines & Immunotherapeutics, 11:1, 288-292, DOI: 10.4161/hv.36166 To link to this article: http://dx.doi.org/10.4161/hv.36166
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Research Paper
Research Paper
Human Vaccines & Immunotherapeutics 11:1, 288–292; January 2015; © 2015 Landes Bioscience
Implication of health care personnel in measles transmission The need for updated immunization status in the move towards eradication of measles in Catalonia
Public Health Agency of Catalonia; Department of Health of the Generalitat of Catalonia; 2CIBER Epidemiología y Salud Pública (CIBERESP); Spain; 3Department of Public Health; University of Barcelona; Spain; 4Public Health Agency of Barcelona; Spain
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1
Keywords: Measles outbreaks, Healthcare Personnel, Immunization, Nosocomial setting, Measles elimination Abbreviations: CI, Confidence Interval; ER, Emergency Room; HC, Health care; HCP, Health care personnel; MMR, MeaslesMumps-Rubella Vaccine; MCV, Measles Containing Vaccine; MV, Measles Virus; mo, month; OR, Odds ratio; y, year
Healthcare personnel (HCP) play an important role in transmission of highly contagious diseases such as measles. Current immunization guidelines in Catalonia include Measles-Mumps-Rubella (MMR) immunization for HCP born after 1967 without evidence of immunity. Despite high vaccination coverage (90%) a high burden of measles cases related to outbreaks have occurred. The aim of this study was to assess the implication of HCP in measles transmission related to healthcare setting. A review of surveillance case data from 2001 to 2013 gathered through the Measles Elimination Program in Catalonia was performed. Twenty six outbreaks involving 797 cases were reported, 52 (6.5%) were HCP aged 21–41 years, 72,5% (38) patient were care personnel (doctors and nurses) and 22,5% (14) other health care related personnel. Forty six 87%) were unvaccinated, 4(10%) had only one dose and 2 had two doses of MMR. In community outbreaks 30 clusters with HCP involved were observed, yet none were identified as index cases. Non-vaccinated HCPs against measles were all under 45 years of age. Vaccination is the only reliable protection against nosocomial spread of measles from HCPs. Assessing vaccination status of HCPs and implementing a 2 dose vaccination in those lacking evidence of immunity is needed in order to set to zero the risk of acquiring and spreading measles in healthcare (HC) settings.
Introduction Healthcare personnel (HCP) play an important role in the transmission of contagious pathogens in the healthcare setting. As such, HCP immunization is a foundational practice, in combination with basic infection control measures such as hand hygiene and use of isolation precautions, to prevent healthcare-associated transmission of pathogens to patients and coworkers and to protect the individual HCP from morbidity. Recommendation for immunization of HCP centers upon several core concepts which take into account the role HCP play in healthcare-associated pathogen transmission to their patients and other HCP as well as increased personal risk for infection. Recently, nosocomial outbreaks of vaccine-preventable infections in which HCP were implicated as the index case have become extensive, underscoring this pivotal role of HCP in disease transmission.1 Furthermore, atypical presentations of measles may also delay the diagnosis2
and implementation of adequate isolation procedures. Other issues to take into account are presenteeism and absenteeism of unimmunized HCP who contract a vaccine-preventable illness while not responsible for pathogen transmission in a healthcare facility. The former, working while ill, shows the desire not to burden colleagues to cover a shift, and an overriding responsibility to care for the individual’s patients, and the latter can also negatively impact patient safety by increasing nurse-to-patient ratios and requiring temporary HCP to perform patient care in an unfamiliar environment.3,4 Moreover, in countries and regions where measles has been either eliminated or significantly reduced, such is the case of Catalonia,5 the index of suspicion among health care personnel (HCP) has declined, and nosocomial transmission has become more frequent. Measles is one of the most readily transmitted communicable diseases, with a basic reproduction number ranging from 7.7 to 15.6 Despite this fact, it is a disease for which conditions for
*Correspondence to: Nuria Torner; Email: [email protected] Submitted: 06/30/2014; Accepted: 07/08/2014; Published Online: 08/28/2014 http://dx.doi.org/10.4161/hv.36166 www.landesbioscience.com Human Vaccines & Immunotherapeutics 288
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Núria Torner1,2,3,*, Ruben Solano2,3, Cristina Rius2,4, Angela Domínguez2,3, and the Measles Elimination Program Surveillance Network of Catalonia, Spain
Results During the study period, 26 outbreaks involving 797 cases were reported; of these 52 (6.5%) were HCP (72.5% (38) patient care personnel (doctors and nurses) and 22.5% (14) other health care related personnel. Thirty clusters of HCP associated cases were identified with a total of 158 cases, which represent 19.8% of all cases confirmed during the period from 2001–2013. During this period, the proportion of HCP involved in outbreaks showed a raising trend ranging from 2.9% to 5.4% during the study period (Fig. 1) In 86.7% of clusters the transmission setting corresponded to hospital facilities, 2 in primary health care setting and 2 in other community health care facilities. Only one HCP was identified as a vehicle of transmission to 2 community members outside the HC setting. According to gender and age distribution of HCP, 62.5% were women; 92.3% aged between 25–44 y (55.8% 25–34 y and 36.5% from 35–44 y). Forty six cases (87%) were unvaccinated, 4(10%) had only one dose and 2 had two doses of MMR. Non-vaccinated HCPs against measles were all under 45 y of age. There was no statistically significant difference between the rate of unproperly vaccinated and unvaccinated physicians (90%) and nursing staff (100%) [(OR:0.35; 95%CI:0.04–4.47); P = 0.61]. Forty eight of the cases in HCP were in the hospital setting (92.3%), whereas only 4 occurred in community primary care setting. Those occurring in the hospital setting affected ER services and in one case an oncology ward. There was no statistical difference in the proportion of men and women classified as patient care personnel and health related personnel [(OR:0.28; 95%CI:0.07–1.15); P = 0.09].
Discussion
Figure 1. Proportion of HCP involved in mealses outbreaks. Catalonia, 2001-2013. 2 Human Vaccines & Immunotherapeutics
Healthcare personnel play a pivotal role in the transmission of contagious pathogens in the healthcare setting and also in the community because of their close contact with patients they can act as pathogen transmission vectors as well as be at increased risk for infection themselves. Despite the availability of an effective and safe vaccine for almost half a century, measles is re-emerging in several developed countries because of the insufficient vaccination coverage among specific subpopulations, the emerging anti-vaccination movement, and the increasing movement of humans across borders. In this context, healthcare settings play a critical role
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eradication are favorable: humans are the only reservoir for the measles virus (MV), the vaccine is safe, inexpensive and produces life-long immunity, diagnostic tests are both specific and sensitive, all infected people develop symptoms, and there are no chronic carriers.7,8 Eradicating measles would represent a major public health achievement, well worth the investment it requires. For the European Region, the first step towards eradication of measles is effective control within its own borders. Measles cases in this region have been increasing in the last decade; this illustrates the challenge of what we are now encountering in the form of pediatric preventable diseases. Despite overall high vaccination coverage, measles continues to cause frequent outbreaks.9-12 The risk of acquiring measles is estimated to be 13 to 19 times higher for susceptible HCP than for the general population. Thus, continued awareness and efforts are needed and especial efforts should be set on the importance of nosocomial transmission.13 In Catalonia, a region in the northeast of Spain with a population of more than 7.5 million inhabitants, autochthonous measles was declared eliminated in the year 20005 as the result of high Measles Mumps Rubella vaccine (MMR) coverage for first and second dose (15 mo and 4 y) since mid-90s. Although sporadic imported cases and small outbreaks have appeared, it wasn’t until 2006 when a large measles outbreak affecting mostly unvaccinated toddlers stroke the Barcelona Health Region. After this event, there have been other significantly important outbreaks.14,15 The aim of this study was to assess the implication of HCP in measles transmission related to healthcare setting in the years following autochthonous measles elimination in Catalonia.
HCPs, France for HCPs in direct patient care, and Austria for pediatricians only. In Finland, HCP vaccination against measles is mandatory. No recommendations for HCP vaccination against measles are in place in the remaining 15 countries members of the European Union.23 The criteria accepted as sufficient evidence of immunity in the general population may be insufficient in HCW, especially in younger age groups. These criteria should be reviewed, replacing the required documentation of physician-diagnosed disease as an evidence of measles immunity by laboratory confirmation of measles.24-26 Those HCP who cannot provide proof of laboratoryconfirmed measles or receipt of two doses of MCV should receive two doses of MMR separated by an interval of 28 d or more. Although most HCP have immunity against measles, everybody working in medical facilities should have evidence of this immunity. It should be mandatory to identify non-immune HCP and offer them vaccination. Only HCP who are vaccinated or willing to be vaccinated should be recruited to work on medical wards, especially high risk wards such as infectious disease unit, emergency room, intensive care and critical care units, and pediatric, maternity and oncology wards. There are some limitations to the study due to the observational nature of this study, we cannot exclude biases. We used an estimation approach to link cases to nosocomial setting (incubation period and spatial closeness approximation) to detect possibly related cases and took HCP as index case or secondary case and vector for transmission in an ongoing community outbreak setting. In the current era of frequent international travel, surveillance is required to ensure that appropriate, common sense infection control procedures are in place, including enforcement of policies preventing health care staff from working while they are potentially infectious.3,12,25 Furthermore, a policy that ensures adequate coverage may be cost-effective for health care institutions by mitigating the negative financial impact associated with nosocomial outbreaks. There is evidence that decreased bed occupancy rates result in greater costs to the institution than costs from infection control or diagnostic measures.27 Eliminating measles by 2010 has not been accomplished. Stronger recommendations and higher vaccination coverage against measles in health-care workers including medical students and health care related personnel, could contribute to eliminate measles in the general population. If mandatory vaccination is not possible in Catalonia, a strategy of voluntary vaccination for HCP should be rapidly implemented in hospitals, especially in high risk areas and even on infectious disease wards where isolation barriers are usually used carefully.28 According to Ajenjo et al., the most successful interventions were adding influenza vaccination rates to the quality scorecard incentive program and the use of declination statements to improve vaccination uptake.29 Vaccination is the only reliable protection against nosocomial spread of measles from HCPs. Assessing vaccination status of HCPs and implementing 2 dose vaccination in those lacking evidence of immunity is needed in order to set to zero the risk of acquiring and spreading measles in health-care settings.
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in the transmission of infection and generation of cases. Healthcare-associated outbreaks may be associated with severe morbidity and mortality among specific groups of patients, disruption of health-care services, and considerable costs. In our study one of the physicians infected while on duty at the ER ward, also worked in the oncology ward with immunosuppresed patients. This originated susceptible contact tracing among more than 100 patients and other HCP ending in emergency serological testing and administration of standard immunoglobulin to approximately 10% of the contacts. The fact that patients were mainly older adults with low susceptibility to measles diminished the severity and costs, but this was only circumstantial because the event could have occurred in a ward with a greater number of susceptible immunocompromised patients. Misdiagnosis or delayed diagnosis of a measles, as in this study, and inadequate implementation of infection control measures are common in almost all events of nosocomial spread. Measles vaccination of healthcare workers is an effective means of prevention of nosocomial measles outbreaks. The fact that cases with two doses of MMR vaccine occurred has also been described by other authors as having occurred in the peak activity of ongoing outbreaks which rely on correctly vaccinated physicians to attend patients suspected of measles.16 Yet, the absence or reduced severity of respiratory symptoms, particularly a cough, may result in lower infectivity relative to a classic measles infection.17,18 Over the last decade several countries have made efforts to build infection control capacity within health-care facilities to improve HCP and patient safety. Vaccination is the only reliable protection against nosocomial spread of measles. Reports of susceptibility to measles showed a high level of immunity, including natural immunity, among HCP in Europe.19 However, this was not confirmed by the results of a study conducted in Catalonia, which showed that the most susceptible group was among HCP born after 1980, who should have received two doses of MCV. In our study we found that cases in HCP were mostly (55.8%) in the 25–34 y age group in concordance with the fore mentioned susceptibility study.20 These findings are similar to those of Botelho-Nevers et al.1 suggesting that, in younger subjects, vaccination coverage remained low. Therefore, even if the prevalence of non-immune HCP seems to be low, the low uptake of MMR immunization and the appearance of measles outbreaks increase the risk of nosocomial transmission as seen in the rising trend observed in large outbreaks occurred in Catalonia during the study period. Nevertheless, the percentage of HCP involved is much lower than in other countries where the percentage of HCP affected reached 12% in France and almost 10% in Bulgaria.1,21 Vaccination of HCPs at risk constitutes a major infection prevention measure against measles. It is justified by the necessity to protect them, but also to indirectly protect their susceptible patients, who themselves may not be able to develop protective immunity after vaccination (e.g., immunocompromised patients), may not be eligible for vaccination (e.g., neonates), or who may simply be unvaccinated or oppose vaccination.22 Twelve countries (Belgium, Cyprus, Germany, Ireland, Italy, Lithuania, Luxemburg, Malta, Russia, Spain, Switzerland, and United Kingdom) recommend measles vaccination for all
Material and Methods
Disclosure of Potential Conflicts of Interest
References 1. Botelho-Nevers E, Cassir N, Minodier P, Laporte R, Gautret P, Badiaga S, Thiberville DJ, Ninove L, Charrel R, Brouqui P. Measles among healthcare workers: a potential for nosocomial outbreaks. Euro Surveill 2011; 16:16; PMID:21251488 2. Lupo J, Bernard S, Wintenberger C, Baccard M, Vabret A, Antona D, Timsit JF, Morand P. Fatal measles without rash in immunocompetent adult, France. Emerg Infect Dis 2012; 18:521-3; PMID:22377448; http://dx.doi.org/10.3201/eid1803.111300 3. Widera E, Chang A, Chen HL. Presenteeism: a public health hazard. J Gen Intern Med 2010; 25:12447; PMID:20549378; http://dx.doi.org/10.1007/ s11606-010-1422-x 4. Talbot TR. Update on immunizations for healthcare personnel in the United States. Vaccine 2014; 32:4869-75; PMID:24231439 5. Salleras L, Dominguez A, Torner N. Confirmed interruption of indigenous measles transmission in Catalonia. Euro Surveill 2001; 6:113-7 6. Mossong J, Muller CP. Estimation of the basic reproduction number of measles during an outbreak in a partially vaccinated population. Epidemiol Infect 2000; 124:273-8; PMID:10813153; http://dx.doi. org/10.1017/S0950268899003672 7. World Health Organization. Proceedings of the Global Technical Consultation to assess the feasibility of measles eradication, 28-30 July 2010. J Infect Dis 2011; 204(Suppl 1):S4-13; PMID:21666191; http://dx.doi.org/10.1093/infdis/jir100 8. Moss WJ, Strebel P. Biological feasibility of measles eradication. J Infect Dis 2011; 204(Suppl 1):S47-53; PMID:21666201; http://dx.doi.org/10.1093/infdis/ jir065 9. Bassetti M, Schenone E, Calzi A, Camera M, Valle L, Ansaldi F, Pagano G, Viscoli C. Measles outbreak in adults in Italy. Infez Med 2011; 19:16-9; PMID:21471742 10. Benkimoun P. Outbreak of measles in France shows no signs of abating. BMJ 2011; 342:d3161; PMID:21602242; http://dx.doi.org/10.1136/bmj. d3161
Acknowledgements
We thank all reporting physicians and the other members of the Measles Elimination Program Surveillance Network of Catalonia: Alseda M, Alvarez J, Arias C, Artigues A, Balaña PJ, Carmona G, Carol M, Ciruela P, Company M, Follia N, Godoy P, Hernandez S, Izquierdo C, Martinez A, Plasencia E, Recasens A, Rodes A, Rovira A, Ruiz L, Sala MR, Torres J (Public Health Agency of Catalonia), and Caylà J, Manzanares S, Santomà MJ, Clos, R Masdeu E, Simon P, Garcia R, Gorrindo P (Public Health Agency of Barcelona), and Costa J, Isanta R and Mosquera MM (Service of Microbiology, H Clinic of Barcelona). Financial Disclosure
This work was partially supported by the Agency for the Management of Grants for University Research (AGAUR Grant number 2014 SAGR 1403) and CIBER Epidemiology and Public Health (CIBERESP).
11. Delgado de Los Reyes J, Arencibia JM, Navarro GJ, Alonso EE, Garcia PP, Banqueri GE, et al. Ongoing measles outbreak in Elche, Spain, 29 January to 9 March 2012. Euro Surveill 2012;17. 12. Kantele A, Valtonen K, Davidkin I, Martelius T, Võželevskaja N, Skogberg K, Liesmaa I, Lyytikäinen O. Travellers returning with measles from Thailand to Finland, April 2012: infection control measures. Euro Surveill 2012; 17:17; PMID:22687913 13. Botelho-Nevers E, Gautret P, Biellik R, Brouqui P. Nosocomial transmission of measles: an updated review. Vaccine 2012; 30:3996-4001; PMID:22521843; http://dx.doi.org/10.1016/j. vaccine.2012.04.023 14. Domínguez A, Torner N, Barrabeig I, Rovira A, Rius C, Cayla J, Plasencia E, Minguell S, Sala MR, Martínez A, et al.; Working Group for the Study of the Measles Outbreak in Catalonia. Large outbreak of measles in a community with high vaccination coverage: implications for the vaccination schedule. Clin Infect Dis 2008; 47:1143-9; PMID:18823269; http://dx.doi.org/10.1086/592258 15. Torner N, Anton A, Barrabeig I, Lafuente S, Parron I, Arias C, Camps N, Costa J, Martínez A, Torra R, et al.; Measles Elimination Program Surveillance Network of Catalonia, Spain. Epidemiology of two large measles virus outbreaks in Catalonia: what a difference the month of administration of the first dose of vaccine makes. Hum Vaccin Immunother 2013; 9:675-80; PMID:23303107; http://dx.doi. org/10.4161/hv.23265 16. Rota JS, Hickman CJ, Sowers SB, Rota PA, Mercader S, Bellini WJ. Two case studies of modified measles in vaccinated physicians exposed to primary measles cases: high risk of infection but low risk of transmission. J Infect Dis 2011; 204(Suppl 1):S559-63; PMID:21666213; http://dx.doi.org/10.1093/infdis/ jir098 17. Aaby P, Bukh J, Leerhøy J, Lisse IM, Mordhorst CH, Pedersen IR. Vaccinated children get milder measles infection: a community study from Guinea-Bissau. J Infect Dis 1986; 154:858-63; PMID:3772165; http://dx.doi.org/10.1093/infdis/154.5.858
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18. Lee MS, Nokes DJ, Hsu HM, Lu CF. Protective titres of measles neutralising antibody. J Med Virol 2000; 62:511-7; PMID:11074481; http://dx.doi. org/10.1002/1096-9071(200012)62:43.0.CO;2-Z 19. Fedeli U, Zanetti C, Saia B. Susceptibility of healthcare workers to measles, mumps rubella and varicella. J Hosp Infect 2002; 51:133-5; PMID:12090801; http://dx.doi.org/10.1053/jhin.2002.1222 20. Urbiztondo L, Borràs E, Costa J, Broner S, Campins M, Bayas JM, Esteve M, Domínguez A; Working Group for the Study of the Immune Status in Healthcare Workers in Catalonia. Prevalence of measles antibodies among health care workers in Catalonia (Spain) in the elimination era. BMC Infect Dis 2013; 13:391; PMID:23978316; http://dx.doi. org/10.1186/1471-2334-13-391 21. Komitova R, Kunchev A, Mihneva Z, Marinova L. Nosocomial transmission of measles among healthcare workers, Bulgaria, 2010. Euro Surveill 2011; 16:16; PMID:21507322 22. Poland GA, Jacobson RM. The age-old struggle against the antivaccinationists. N Engl J Med 2011; 364:97-9; PMID:21226573; http://dx.doi. org/10.1056/NEJMp1010594 23. Maltezou HC, Fusco FM, Schilling S, De Iaco G, Gottschalk R, Brodt HR, Bannister B, Brouqui P, Thomson G, Puro V, et al.; EuroNHID Working Group. Infection control practices in facilities for highly infectious diseases across Europe. J Hosp Infect 2012; 81:184-91; PMID:22648013; http:// dx.doi.org/10.1016/j.jhin.2012.04.019 24. Centers for Disease Control and Prevention. Recommended adult immunization schedule-United States, 2012. MMWR Recomm Rep 2012; 61:1-7 25. Chen SY, Anderson S, Kutty PK, Lugo F, McDonald M, Rota PA, Ortega-Sanchez IR, Komatsu K, Armstrong GL, Sunenshine R, et al. Health careassociated measles outbreak in the United States after an importation: challenges and economic impact. J Infect Dis 2011; 203:1517-25; PMID:21531693; http://dx.doi.org/10.1093/infdis/jir115
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No potential conflicts of interest were disclosed. Urgent reported suspected cases of measles to the Public Health Surveillance units were registered and data on age, vaccination status, clinical course and epidemiological information relevant to healthcare setting association were obtained by case interviews and review of medical records. A review of surveillance case data from confirmed cases during the post-elimination period, from 2001 to 2013, gathered through the Measles Elimination Program in Catalonia was performed. Definition of HCP included two basic categories: (1) Patient care personnel: Physicians, nursing staff, lab technicians; and (2) Health care related personnel: Ambulance non-medical personnel, admission staff, cleaning and maintenance personnel and other non-medical personnel. Estimation of the number of healthcare associated cases was performed according to recorded date of onset of exanthema and attendance to a healthcare facility where a HCP measles case was identified. Statistical assessment of OR and their 95%CI were determined by Chi2 and Fisher tests. Statistical analysis was performed by means of the SPSS® 18.0 statistical package for windows (SPSS). Statistical significance set at α = 0.05.
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26. Mendelson GM, Roth CE, Wreghitt TG, Brown NM, Ziegler E, Lever AM. Nosocomial transmission of measles to healthcare workers. Time for a national screening and immunization policy for NHS staff? J Hosp Infect 2000; 44:154-5; PMID:10662570; http://dx.doi.org/10.1053/jhin.1999.0667 27. Zingg W, Colombo C, Jucker T, Bossart W, Ruef C. Impact of an outbreak of norovirus infection on hospital resources. Infect Control Hosp Epidemiol 2005; 26:263-7; PMID:15796278; http://dx.doi. org/10.1086/502537 28. Centers for Disease Control and Prevention. Measles: Epidemiology and prevention of vaccine-preventable diseases. 12th edition:173-97 http://www cdc gov/ vaccines/pubs/pinkbook/ 2012 [cited 2014 Apr 15] 29. Ajenjo MC, Woeltje KF, Babcock HM, Gemeinhart N, Jones M, Fraser VJ. Influenza vaccination among healthcare workers: ten-year experience of a large healthcare organization. Infect Control Hosp Epidemiol 2010; 31:233-40; PMID:20055666; http://dx.doi.org/10.1086/650449
ISSN: 2164-5515 (Print) 2164-554X (Online) Journal homepage: http://www.tandfonline.com/loi/khvi20
Implication of health care personnel in measles transmission Núria Torner, Ruben Solano, Cristina Rius, Angela Domínguez & the Measles Elimination Program Surveillance Network of Catalonia, Spain To cite this article: Núria Torner, Ruben Solano, Cristina Rius, Angela Domínguez & the Measles Elimination Program Surveillance Network of Catalonia, Spain (2015) Implication of health care personnel in measles transmission, Human Vaccines & Immunotherapeutics, 11:1, 288-292, DOI: 10.4161/hv.36166 To link to this article: http://dx.doi.org/10.4161/hv.36166
Published online: 01 Nov 2014.
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Article views: 25
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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=khvi20 Download by: [University of California, San Diego]
Date: 06 November 2015, At: 10:45
Research Paper
Research Paper
Human Vaccines & Immunotherapeutics 11:1, 288–292; January 2015; © 2015 Landes Bioscience
Implication of health care personnel in measles transmission The need for updated immunization status in the move towards eradication of measles in Catalonia
Public Health Agency of Catalonia; Department of Health of the Generalitat of Catalonia; 2CIBER Epidemiología y Salud Pública (CIBERESP); Spain; 3Department of Public Health; University of Barcelona; Spain; 4Public Health Agency of Barcelona; Spain
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1
Keywords: Measles outbreaks, Healthcare Personnel, Immunization, Nosocomial setting, Measles elimination Abbreviations: CI, Confidence Interval; ER, Emergency Room; HC, Health care; HCP, Health care personnel; MMR, MeaslesMumps-Rubella Vaccine; MCV, Measles Containing Vaccine; MV, Measles Virus; mo, month; OR, Odds ratio; y, year
Healthcare personnel (HCP) play an important role in transmission of highly contagious diseases such as measles. Current immunization guidelines in Catalonia include Measles-Mumps-Rubella (MMR) immunization for HCP born after 1967 without evidence of immunity. Despite high vaccination coverage (90%) a high burden of measles cases related to outbreaks have occurred. The aim of this study was to assess the implication of HCP in measles transmission related to healthcare setting. A review of surveillance case data from 2001 to 2013 gathered through the Measles Elimination Program in Catalonia was performed. Twenty six outbreaks involving 797 cases were reported, 52 (6.5%) were HCP aged 21–41 years, 72,5% (38) patient were care personnel (doctors and nurses) and 22,5% (14) other health care related personnel. Forty six 87%) were unvaccinated, 4(10%) had only one dose and 2 had two doses of MMR. In community outbreaks 30 clusters with HCP involved were observed, yet none were identified as index cases. Non-vaccinated HCPs against measles were all under 45 years of age. Vaccination is the only reliable protection against nosocomial spread of measles from HCPs. Assessing vaccination status of HCPs and implementing a 2 dose vaccination in those lacking evidence of immunity is needed in order to set to zero the risk of acquiring and spreading measles in healthcare (HC) settings.
Introduction Healthcare personnel (HCP) play an important role in the transmission of contagious pathogens in the healthcare setting. As such, HCP immunization is a foundational practice, in combination with basic infection control measures such as hand hygiene and use of isolation precautions, to prevent healthcare-associated transmission of pathogens to patients and coworkers and to protect the individual HCP from morbidity. Recommendation for immunization of HCP centers upon several core concepts which take into account the role HCP play in healthcare-associated pathogen transmission to their patients and other HCP as well as increased personal risk for infection. Recently, nosocomial outbreaks of vaccine-preventable infections in which HCP were implicated as the index case have become extensive, underscoring this pivotal role of HCP in disease transmission.1 Furthermore, atypical presentations of measles may also delay the diagnosis2
and implementation of adequate isolation procedures. Other issues to take into account are presenteeism and absenteeism of unimmunized HCP who contract a vaccine-preventable illness while not responsible for pathogen transmission in a healthcare facility. The former, working while ill, shows the desire not to burden colleagues to cover a shift, and an overriding responsibility to care for the individual’s patients, and the latter can also negatively impact patient safety by increasing nurse-to-patient ratios and requiring temporary HCP to perform patient care in an unfamiliar environment.3,4 Moreover, in countries and regions where measles has been either eliminated or significantly reduced, such is the case of Catalonia,5 the index of suspicion among health care personnel (HCP) has declined, and nosocomial transmission has become more frequent. Measles is one of the most readily transmitted communicable diseases, with a basic reproduction number ranging from 7.7 to 15.6 Despite this fact, it is a disease for which conditions for
*Correspondence to: Nuria Torner; Email: [email protected] Submitted: 06/30/2014; Accepted: 07/08/2014; Published Online: 08/28/2014 http://dx.doi.org/10.4161/hv.36166 www.landesbioscience.com Human Vaccines & Immunotherapeutics 288
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Núria Torner1,2,3,*, Ruben Solano2,3, Cristina Rius2,4, Angela Domínguez2,3, and the Measles Elimination Program Surveillance Network of Catalonia, Spain
Results During the study period, 26 outbreaks involving 797 cases were reported; of these 52 (6.5%) were HCP (72.5% (38) patient care personnel (doctors and nurses) and 22.5% (14) other health care related personnel. Thirty clusters of HCP associated cases were identified with a total of 158 cases, which represent 19.8% of all cases confirmed during the period from 2001–2013. During this period, the proportion of HCP involved in outbreaks showed a raising trend ranging from 2.9% to 5.4% during the study period (Fig. 1) In 86.7% of clusters the transmission setting corresponded to hospital facilities, 2 in primary health care setting and 2 in other community health care facilities. Only one HCP was identified as a vehicle of transmission to 2 community members outside the HC setting. According to gender and age distribution of HCP, 62.5% were women; 92.3% aged between 25–44 y (55.8% 25–34 y and 36.5% from 35–44 y). Forty six cases (87%) were unvaccinated, 4(10%) had only one dose and 2 had two doses of MMR. Non-vaccinated HCPs against measles were all under 45 y of age. There was no statistically significant difference between the rate of unproperly vaccinated and unvaccinated physicians (90%) and nursing staff (100%) [(OR:0.35; 95%CI:0.04–4.47); P = 0.61]. Forty eight of the cases in HCP were in the hospital setting (92.3%), whereas only 4 occurred in community primary care setting. Those occurring in the hospital setting affected ER services and in one case an oncology ward. There was no statistical difference in the proportion of men and women classified as patient care personnel and health related personnel [(OR:0.28; 95%CI:0.07–1.15); P = 0.09].
Discussion
Figure 1. Proportion of HCP involved in mealses outbreaks. Catalonia, 2001-2013. 2 Human Vaccines & Immunotherapeutics
Healthcare personnel play a pivotal role in the transmission of contagious pathogens in the healthcare setting and also in the community because of their close contact with patients they can act as pathogen transmission vectors as well as be at increased risk for infection themselves. Despite the availability of an effective and safe vaccine for almost half a century, measles is re-emerging in several developed countries because of the insufficient vaccination coverage among specific subpopulations, the emerging anti-vaccination movement, and the increasing movement of humans across borders. In this context, healthcare settings play a critical role
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eradication are favorable: humans are the only reservoir for the measles virus (MV), the vaccine is safe, inexpensive and produces life-long immunity, diagnostic tests are both specific and sensitive, all infected people develop symptoms, and there are no chronic carriers.7,8 Eradicating measles would represent a major public health achievement, well worth the investment it requires. For the European Region, the first step towards eradication of measles is effective control within its own borders. Measles cases in this region have been increasing in the last decade; this illustrates the challenge of what we are now encountering in the form of pediatric preventable diseases. Despite overall high vaccination coverage, measles continues to cause frequent outbreaks.9-12 The risk of acquiring measles is estimated to be 13 to 19 times higher for susceptible HCP than for the general population. Thus, continued awareness and efforts are needed and especial efforts should be set on the importance of nosocomial transmission.13 In Catalonia, a region in the northeast of Spain with a population of more than 7.5 million inhabitants, autochthonous measles was declared eliminated in the year 20005 as the result of high Measles Mumps Rubella vaccine (MMR) coverage for first and second dose (15 mo and 4 y) since mid-90s. Although sporadic imported cases and small outbreaks have appeared, it wasn’t until 2006 when a large measles outbreak affecting mostly unvaccinated toddlers stroke the Barcelona Health Region. After this event, there have been other significantly important outbreaks.14,15 The aim of this study was to assess the implication of HCP in measles transmission related to healthcare setting in the years following autochthonous measles elimination in Catalonia.
HCPs, France for HCPs in direct patient care, and Austria for pediatricians only. In Finland, HCP vaccination against measles is mandatory. No recommendations for HCP vaccination against measles are in place in the remaining 15 countries members of the European Union.23 The criteria accepted as sufficient evidence of immunity in the general population may be insufficient in HCW, especially in younger age groups. These criteria should be reviewed, replacing the required documentation of physician-diagnosed disease as an evidence of measles immunity by laboratory confirmation of measles.24-26 Those HCP who cannot provide proof of laboratoryconfirmed measles or receipt of two doses of MCV should receive two doses of MMR separated by an interval of 28 d or more. Although most HCP have immunity against measles, everybody working in medical facilities should have evidence of this immunity. It should be mandatory to identify non-immune HCP and offer them vaccination. Only HCP who are vaccinated or willing to be vaccinated should be recruited to work on medical wards, especially high risk wards such as infectious disease unit, emergency room, intensive care and critical care units, and pediatric, maternity and oncology wards. There are some limitations to the study due to the observational nature of this study, we cannot exclude biases. We used an estimation approach to link cases to nosocomial setting (incubation period and spatial closeness approximation) to detect possibly related cases and took HCP as index case or secondary case and vector for transmission in an ongoing community outbreak setting. In the current era of frequent international travel, surveillance is required to ensure that appropriate, common sense infection control procedures are in place, including enforcement of policies preventing health care staff from working while they are potentially infectious.3,12,25 Furthermore, a policy that ensures adequate coverage may be cost-effective for health care institutions by mitigating the negative financial impact associated with nosocomial outbreaks. There is evidence that decreased bed occupancy rates result in greater costs to the institution than costs from infection control or diagnostic measures.27 Eliminating measles by 2010 has not been accomplished. Stronger recommendations and higher vaccination coverage against measles in health-care workers including medical students and health care related personnel, could contribute to eliminate measles in the general population. If mandatory vaccination is not possible in Catalonia, a strategy of voluntary vaccination for HCP should be rapidly implemented in hospitals, especially in high risk areas and even on infectious disease wards where isolation barriers are usually used carefully.28 According to Ajenjo et al., the most successful interventions were adding influenza vaccination rates to the quality scorecard incentive program and the use of declination statements to improve vaccination uptake.29 Vaccination is the only reliable protection against nosocomial spread of measles from HCPs. Assessing vaccination status of HCPs and implementing 2 dose vaccination in those lacking evidence of immunity is needed in order to set to zero the risk of acquiring and spreading measles in health-care settings.
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in the transmission of infection and generation of cases. Healthcare-associated outbreaks may be associated with severe morbidity and mortality among specific groups of patients, disruption of health-care services, and considerable costs. In our study one of the physicians infected while on duty at the ER ward, also worked in the oncology ward with immunosuppresed patients. This originated susceptible contact tracing among more than 100 patients and other HCP ending in emergency serological testing and administration of standard immunoglobulin to approximately 10% of the contacts. The fact that patients were mainly older adults with low susceptibility to measles diminished the severity and costs, but this was only circumstantial because the event could have occurred in a ward with a greater number of susceptible immunocompromised patients. Misdiagnosis or delayed diagnosis of a measles, as in this study, and inadequate implementation of infection control measures are common in almost all events of nosocomial spread. Measles vaccination of healthcare workers is an effective means of prevention of nosocomial measles outbreaks. The fact that cases with two doses of MMR vaccine occurred has also been described by other authors as having occurred in the peak activity of ongoing outbreaks which rely on correctly vaccinated physicians to attend patients suspected of measles.16 Yet, the absence or reduced severity of respiratory symptoms, particularly a cough, may result in lower infectivity relative to a classic measles infection.17,18 Over the last decade several countries have made efforts to build infection control capacity within health-care facilities to improve HCP and patient safety. Vaccination is the only reliable protection against nosocomial spread of measles. Reports of susceptibility to measles showed a high level of immunity, including natural immunity, among HCP in Europe.19 However, this was not confirmed by the results of a study conducted in Catalonia, which showed that the most susceptible group was among HCP born after 1980, who should have received two doses of MCV. In our study we found that cases in HCP were mostly (55.8%) in the 25–34 y age group in concordance with the fore mentioned susceptibility study.20 These findings are similar to those of Botelho-Nevers et al.1 suggesting that, in younger subjects, vaccination coverage remained low. Therefore, even if the prevalence of non-immune HCP seems to be low, the low uptake of MMR immunization and the appearance of measles outbreaks increase the risk of nosocomial transmission as seen in the rising trend observed in large outbreaks occurred in Catalonia during the study period. Nevertheless, the percentage of HCP involved is much lower than in other countries where the percentage of HCP affected reached 12% in France and almost 10% in Bulgaria.1,21 Vaccination of HCPs at risk constitutes a major infection prevention measure against measles. It is justified by the necessity to protect them, but also to indirectly protect their susceptible patients, who themselves may not be able to develop protective immunity after vaccination (e.g., immunocompromised patients), may not be eligible for vaccination (e.g., neonates), or who may simply be unvaccinated or oppose vaccination.22 Twelve countries (Belgium, Cyprus, Germany, Ireland, Italy, Lithuania, Luxemburg, Malta, Russia, Spain, Switzerland, and United Kingdom) recommend measles vaccination for all
Material and Methods
Disclosure of Potential Conflicts of Interest
References 1. Botelho-Nevers E, Cassir N, Minodier P, Laporte R, Gautret P, Badiaga S, Thiberville DJ, Ninove L, Charrel R, Brouqui P. Measles among healthcare workers: a potential for nosocomial outbreaks. Euro Surveill 2011; 16:16; PMID:21251488 2. Lupo J, Bernard S, Wintenberger C, Baccard M, Vabret A, Antona D, Timsit JF, Morand P. Fatal measles without rash in immunocompetent adult, France. Emerg Infect Dis 2012; 18:521-3; PMID:22377448; http://dx.doi.org/10.3201/eid1803.111300 3. Widera E, Chang A, Chen HL. Presenteeism: a public health hazard. J Gen Intern Med 2010; 25:12447; PMID:20549378; http://dx.doi.org/10.1007/ s11606-010-1422-x 4. Talbot TR. Update on immunizations for healthcare personnel in the United States. Vaccine 2014; 32:4869-75; PMID:24231439 5. Salleras L, Dominguez A, Torner N. Confirmed interruption of indigenous measles transmission in Catalonia. Euro Surveill 2001; 6:113-7 6. Mossong J, Muller CP. Estimation of the basic reproduction number of measles during an outbreak in a partially vaccinated population. Epidemiol Infect 2000; 124:273-8; PMID:10813153; http://dx.doi. org/10.1017/S0950268899003672 7. World Health Organization. Proceedings of the Global Technical Consultation to assess the feasibility of measles eradication, 28-30 July 2010. J Infect Dis 2011; 204(Suppl 1):S4-13; PMID:21666191; http://dx.doi.org/10.1093/infdis/jir100 8. Moss WJ, Strebel P. Biological feasibility of measles eradication. J Infect Dis 2011; 204(Suppl 1):S47-53; PMID:21666201; http://dx.doi.org/10.1093/infdis/ jir065 9. Bassetti M, Schenone E, Calzi A, Camera M, Valle L, Ansaldi F, Pagano G, Viscoli C. Measles outbreak in adults in Italy. Infez Med 2011; 19:16-9; PMID:21471742 10. Benkimoun P. Outbreak of measles in France shows no signs of abating. BMJ 2011; 342:d3161; PMID:21602242; http://dx.doi.org/10.1136/bmj. d3161
Acknowledgements
We thank all reporting physicians and the other members of the Measles Elimination Program Surveillance Network of Catalonia: Alseda M, Alvarez J, Arias C, Artigues A, Balaña PJ, Carmona G, Carol M, Ciruela P, Company M, Follia N, Godoy P, Hernandez S, Izquierdo C, Martinez A, Plasencia E, Recasens A, Rodes A, Rovira A, Ruiz L, Sala MR, Torres J (Public Health Agency of Catalonia), and Caylà J, Manzanares S, Santomà MJ, Clos, R Masdeu E, Simon P, Garcia R, Gorrindo P (Public Health Agency of Barcelona), and Costa J, Isanta R and Mosquera MM (Service of Microbiology, H Clinic of Barcelona). Financial Disclosure
This work was partially supported by the Agency for the Management of Grants for University Research (AGAUR Grant number 2014 SAGR 1403) and CIBER Epidemiology and Public Health (CIBERESP).
11. Delgado de Los Reyes J, Arencibia JM, Navarro GJ, Alonso EE, Garcia PP, Banqueri GE, et al. Ongoing measles outbreak in Elche, Spain, 29 January to 9 March 2012. Euro Surveill 2012;17. 12. Kantele A, Valtonen K, Davidkin I, Martelius T, Võželevskaja N, Skogberg K, Liesmaa I, Lyytikäinen O. Travellers returning with measles from Thailand to Finland, April 2012: infection control measures. Euro Surveill 2012; 17:17; PMID:22687913 13. Botelho-Nevers E, Gautret P, Biellik R, Brouqui P. Nosocomial transmission of measles: an updated review. Vaccine 2012; 30:3996-4001; PMID:22521843; http://dx.doi.org/10.1016/j. vaccine.2012.04.023 14. Domínguez A, Torner N, Barrabeig I, Rovira A, Rius C, Cayla J, Plasencia E, Minguell S, Sala MR, Martínez A, et al.; Working Group for the Study of the Measles Outbreak in Catalonia. Large outbreak of measles in a community with high vaccination coverage: implications for the vaccination schedule. Clin Infect Dis 2008; 47:1143-9; PMID:18823269; http://dx.doi.org/10.1086/592258 15. Torner N, Anton A, Barrabeig I, Lafuente S, Parron I, Arias C, Camps N, Costa J, Martínez A, Torra R, et al.; Measles Elimination Program Surveillance Network of Catalonia, Spain. Epidemiology of two large measles virus outbreaks in Catalonia: what a difference the month of administration of the first dose of vaccine makes. Hum Vaccin Immunother 2013; 9:675-80; PMID:23303107; http://dx.doi. org/10.4161/hv.23265 16. Rota JS, Hickman CJ, Sowers SB, Rota PA, Mercader S, Bellini WJ. Two case studies of modified measles in vaccinated physicians exposed to primary measles cases: high risk of infection but low risk of transmission. J Infect Dis 2011; 204(Suppl 1):S559-63; PMID:21666213; http://dx.doi.org/10.1093/infdis/ jir098 17. Aaby P, Bukh J, Leerhøy J, Lisse IM, Mordhorst CH, Pedersen IR. Vaccinated children get milder measles infection: a community study from Guinea-Bissau. J Infect Dis 1986; 154:858-63; PMID:3772165; http://dx.doi.org/10.1093/infdis/154.5.858
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18. Lee MS, Nokes DJ, Hsu HM, Lu CF. Protective titres of measles neutralising antibody. J Med Virol 2000; 62:511-7; PMID:11074481; http://dx.doi. org/10.1002/1096-9071(200012)62:43.0.CO;2-Z 19. Fedeli U, Zanetti C, Saia B. Susceptibility of healthcare workers to measles, mumps rubella and varicella. J Hosp Infect 2002; 51:133-5; PMID:12090801; http://dx.doi.org/10.1053/jhin.2002.1222 20. Urbiztondo L, Borràs E, Costa J, Broner S, Campins M, Bayas JM, Esteve M, Domínguez A; Working Group for the Study of the Immune Status in Healthcare Workers in Catalonia. Prevalence of measles antibodies among health care workers in Catalonia (Spain) in the elimination era. BMC Infect Dis 2013; 13:391; PMID:23978316; http://dx.doi. org/10.1186/1471-2334-13-391 21. Komitova R, Kunchev A, Mihneva Z, Marinova L. Nosocomial transmission of measles among healthcare workers, Bulgaria, 2010. Euro Surveill 2011; 16:16; PMID:21507322 22. Poland GA, Jacobson RM. The age-old struggle against the antivaccinationists. N Engl J Med 2011; 364:97-9; PMID:21226573; http://dx.doi. org/10.1056/NEJMp1010594 23. Maltezou HC, Fusco FM, Schilling S, De Iaco G, Gottschalk R, Brodt HR, Bannister B, Brouqui P, Thomson G, Puro V, et al.; EuroNHID Working Group. Infection control practices in facilities for highly infectious diseases across Europe. J Hosp Infect 2012; 81:184-91; PMID:22648013; http:// dx.doi.org/10.1016/j.jhin.2012.04.019 24. Centers for Disease Control and Prevention. Recommended adult immunization schedule-United States, 2012. MMWR Recomm Rep 2012; 61:1-7 25. Chen SY, Anderson S, Kutty PK, Lugo F, McDonald M, Rota PA, Ortega-Sanchez IR, Komatsu K, Armstrong GL, Sunenshine R, et al. Health careassociated measles outbreak in the United States after an importation: challenges and economic impact. J Infect Dis 2011; 203:1517-25; PMID:21531693; http://dx.doi.org/10.1093/infdis/jir115
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No potential conflicts of interest were disclosed. Urgent reported suspected cases of measles to the Public Health Surveillance units were registered and data on age, vaccination status, clinical course and epidemiological information relevant to healthcare setting association were obtained by case interviews and review of medical records. A review of surveillance case data from confirmed cases during the post-elimination period, from 2001 to 2013, gathered through the Measles Elimination Program in Catalonia was performed. Definition of HCP included two basic categories: (1) Patient care personnel: Physicians, nursing staff, lab technicians; and (2) Health care related personnel: Ambulance non-medical personnel, admission staff, cleaning and maintenance personnel and other non-medical personnel. Estimation of the number of healthcare associated cases was performed according to recorded date of onset of exanthema and attendance to a healthcare facility where a HCP measles case was identified. Statistical assessment of OR and their 95%CI were determined by Chi2 and Fisher tests. Statistical analysis was performed by means of the SPSS® 18.0 statistical package for windows (SPSS). Statistical significance set at α = 0.05.
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26. Mendelson GM, Roth CE, Wreghitt TG, Brown NM, Ziegler E, Lever AM. Nosocomial transmission of measles to healthcare workers. Time for a national screening and immunization policy for NHS staff? J Hosp Infect 2000; 44:154-5; PMID:10662570; http://dx.doi.org/10.1053/jhin.1999.0667 27. Zingg W, Colombo C, Jucker T, Bossart W, Ruef C. Impact of an outbreak of norovirus infection on hospital resources. Infect Control Hosp Epidemiol 2005; 26:263-7; PMID:15796278; http://dx.doi. org/10.1086/502537 28. Centers for Disease Control and Prevention. Measles: Epidemiology and prevention of vaccine-preventable diseases. 12th edition:173-97 http://www cdc gov/ vaccines/pubs/pinkbook/ 2012 [cited 2014 Apr 15] 29. Ajenjo MC, Woeltje KF, Babcock HM, Gemeinhart N, Jones M, Fraser VJ. Influenza vaccination among healthcare workers: ten-year experience of a large healthcare organization. Infect Control Hosp Epidemiol 2010; 31:233-40; PMID:20055666; http://dx.doi.org/10.1086/650449
