ABSTRACT

Objectives.

To assess the accumulated knowledge of the effects of public health emergencies of international concern on disease control and local health systems, and contribute to a better understanding of their effects on health programs and systems.

Methods.

This was a systematic review of published and gray literature (in English, Portuguese, or Spanish). Electronic databases (BVS/LILACS, PubMed, and SciELO) and Google Scholar were searched. Search terms were: COVID-19 OR H1N1 OR Ebola OR Zika OR poliomyelitis AND (outbreaks OR epidemics) AND (public health systems OR public health surveillance).

Results.

A total of 3 508 studies were retrieved, of which 31 met the inclusion criteria. The studies addressed the effects of the emergencies on: communicable diseases notification systems; malaria, HIV/AIDS, tuberculosis, poliomyelitis, and malaria surveillance, control, and treatment; microcephaly; dengue; and vaccinations. The populations affected by the emergencies experienced reduced health services, which included fewer health visits, failures in the diagnostic chain, decrease in vaccination, and increased incidence or underreporting of notifiable diseases.

Conclusions.

Socioeconomic inequity is a determinant of the effects of public health emergencies of international concern within affected populations. The diversion of resources and attention from health authorities disproportionately affects vulnerable populations and can lead, over time, to a weakening of health systems. The analysis of the effects of public health emergencies is important for the development of new protocols that can better respond to future crises.

Keywords
Disease outbreaks; communicable diseases; health care delivery; health systems

RESUMEN

Objetivos.

Evaluar el conocimiento acumulado acerca de los efectos de las emergencias de salud pública de importancia internacional en el control de enfermedades y en los sistemas de salud locales, y contribuir a una mejor comprensión de estos efectos en los programas y sistemas de salud.

Métodos.

Se hizo una revisión sistemática de bibliografía gris y publicada (en español, inglés o portugués) para la que se realizaron búsquedas en bases de datos electrónicas (BVS/LILACS, PubMed y SciELO) y en Google Scholar. Los términos de búsqueda fueron: COVID-19 OR H1N1 OR Ebola OR Zika OR poliomyelitis AND (Outbreaks OR epidemics) AND (public health systems OR public health surveillance).

Resultados.

Se encontraron 3 508 estudios, de los cuales 31 cumplieron los criterios de inclusión. En los estudios se abordaban los efectos de las emergencias en: los sistemas de notificación de enfermedades transmisibles; la vigilancia, el control y el tratamiento de la malaria, el VIH/sida, la tuberculosis y la poliomielitis; la microcefalia; el dengue; y las vacunas. Las poblaciones afectadas por las emergencias experimentaron una reducción de los servicios de salud, incluida una reducción de las consultas de salud, errores en la cadena de diagnóstico, una disminución de la vacunación y el aumento de la incidencia o subnotificación de enfermedades de notificación obligatoria.

Conclusiones.

La inequidad socioeconómica es un determinante de los efectos de las emergencias de salud pública de importancia internacional en los grupos poblacionales afectados. El desvío de recursos y atención de las autoridades de salud afecta desproporcionadamente a los grupos vulnerables y puede suponer, con el tiempo, un debilitamiento de los sistemas de salud. El análisis de los efectos de las emergencias de salud pública es crucial para la elaboración de nuevos protocolos que puedan mejorar la respuesta ante futuras crisis.

Palabras clave
Brotes de enfermedades; enfermedades transmisibles; atención a la salud; sistemas de salud

RESUMO

Objetivos.

Avaliar o conhecimento acumulado sobre os efeitos das emergências de saúde pública de importância internacional no controle de doenças e nos sistemas de saúde locais e contribuir para uma melhor compreensão desses efeitos sobre os programas e sistemas de saúde.

Métodos.

Trata-se de uma revisão sistemática da literatura branca e cinzenta (em inglês, português ou espanhol) realizada por meio de pesquisas nos bancos de dados eletrônicos BVS/LILACS, PubMed e SciELO e no Google Scholar. Foram utilizados os seguintes termos de busca: COVID-19 OR H1N1 OR Ebola OR Zika OR poliomyelitis AND (outbreaks OR epidemics) AND (public health systems OR public health surveillance).

Resultados.

Foi identificado um total de 3 508 estudos, dos quais 31 preencheram os critérios de inclusão. Os estudos abordavam os efeitos das emergências sobre: sistemas de notificação de doenças transmissíveis; vigilância, controle e tratamento de HIV/AIDS, tuberculose, poliomielite e malária; microcefalia; dengue; e vacinações. As populações afetadas pelas emergências enfrentaram uma redução nos serviços de saúde, como menos consultas médicas, problemas na cadeia de diagnóstico, diminuição da vacinação e maior incidência ou subnotificação de doenças de notificação compulsória.

Conclusões.

A desigualdade socioeconômica é um fator determinante dos efeitos das emergências de saúde pública de importância internacional nas populações afetadas. O desvio dos recursos e da atenção das autoridades sanitárias afeta desproporcionalmente as populações vulneráveis e pode levar, com o passar do tempo, a um enfraquecimento dos sistemas de saúde. A análise dos efeitos das emergências de saúde pública é importante para a elaboração de novos protocolos que possam enfrentar melhor futuras crises.

Palavras-chave
Surtos de doenças; doenças transmissíveis; atenção à saúde; sistemas de saúde

Public health emergencies of international concern (PHEIC) are defined by the World Health Organization (WHO) in the International Health Regulations (IHR) as extraordinary public health events, which constitute a risk of dissemination between different states, and which potentially require a coordinated international response (¹1. World Health Organization. International Health Regulations [Internet]. Geneva: WHO 2005 [cited 2022 Apr 27] Available at: https://apps.who.int/iris/bitstream/handle/10665/246107/9789241580496-eng.pdf
https://apps.who.int/iris/bitstream/hand... ). Since the introduction of the new version of the IHR, which was implemented in 2007, six international emergencies have been declared: H1N1, from April 2009 to August 2010; poliovirus, in 2014; Ebola virus, from 2014 to March 2016 and from July 2019 to June 2020; Zika virus, from February to November 2016; and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), in 2020 (²2. World Health Organization. IHR emergency committees [Internet]. Geneva: WHO [cited 2022 Apr 27]. Available at: https://www.who.int/teams/ihr/ihr-emergency-committees
https://www.who.int/teams/ihr/ihr-emerge... ).

In addition to requiring international coordinated action, PHEIC also have the potential to overwhelm health professionals and health systems in affected countries. As such, PHEIC can have severe syndemic consequences for health care and surveillance, and the control of local endemic diseases (³3. Hotez PJ. Neglected tropical diseases in the Ebola-affected countries of West Africa. PLoS Negl Trop Dis. 2015;9:e0003671–⁶6. Júnior JPB, Santos DB. COVID-19 como sindemia: modelo teórico e fundamentos para a abordagem abrangente em saúde. Cad Saúde Pública. 2021;37:e00119021.).

Despite the public health importance of PHEIC, no systematic literature reviews have been done on the effects of such emergencies on disease control and health systems. Therefore, the present study aimed to assess the accumulated knowledge in this field and contribute to a better understanding of the effects of PHEIC on health programs and systems in different contexts in the countries where they occurred.

METHODS

Protocol registration

This was a systematic review registered in the International Prospective Register of Systematic Reviews (PROSPERO), number CRD42021257860 (⁷7. PROSPERO. International Prospective Register of Systematic Reviews [Internet] [cited 2022 Apr 27]. Available at: https://www.crd.york.ac.uk/prospero/display_record.php?RecordID=257860
https://www.crd.york.ac.uk/prospero/disp... ). The review followed the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (⁸8. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.).

Selection and eligibility criteria

In this systematic review, we sought to answer the question: how have PHEIC affected disease surveillance and/or control and health systems in the countries or regions where they occurred?

Criteria for inclusion in this review were: original articles that addressed the effects of active PHEIC on health systems in relation to notifiable diseases; and published in English, Portuguese, or Spanish. No restrictions were put on study design, country, or disease notifiied. For Zika virus, even though the PHEIC was declared because of the association between Zika virus and congenital malformations, studies that either addressed this relationship or the relationship between Zika virus and other diseases were considered for this review.

Selection of studies

Electronic databases were searched on May 27, 2021 for relevant studies. A search was also done on February 18, 2022 to update with new studies. The electronic databases were: Biblioteca Virtural de Saúde (BVS)/Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS), PubMed (via MEDLINE), and Scientific Electronic Library Online (SciELO). Google Scholar was also searched to retrieve relevant gray literature. The search terms were: COVID-19 OR H1N1 OR Ebola OR Zika OR poliomyelitis AND (outbreaks OR epidemics) AND (public health systems OR public health surveillance). The descriptors used were based on the Medical Subject Headings (MeSH) and Health Sciences Descriptors (Descritores em Ciências da Saúde – DeCS).

After exclusion of duplicate articles using Zotero software, the remaining studies were assessed by three independent researchers, first by title and abstract and then by full text. The researchers met to discuss disagreements and another researcher was consulted when a consensus could not be reached.

Assessment of the methodological quality

The studies included in this review were ecological, cross-sectional, and cohort studies, and case reports. Their methodological rigor was assessed using the critical appraisal checklist tool of the Joanna Briggs Institute (⁹9. Moola S, Munn Z, Tufanaru C, Aromataris E, Sears K, Sfetc R, et al. Chapter 7. Systematic reviews of etiology and risk. In: Aromataris E, Munn Z, Editors. JBI manual for evidence synthesis. Adelaide: JBI; 2020 [cited 2022 Apr 27]. Available at: https://synthesismanual.jbi.global
https://synthesismanual.jbi.global... ). Ecological studies were not evaluated for rigor as no relevant tools were available. Each criterion was classified as “yes”, “no”, “uncertain”, or “not applicable”. Studies with one to three “yeses” were considered to have a high risk of bias, four to six “yeses”, a moderate risk of bias, and seven to 11, a low risk of bias (¹⁰10. Mecenas P, Bastos RTDRM, Vallinoto ACR, Normando D. Effects of temperature and humidity on the spread of COVID-19: a systematic review. PLoS One. 2020;15:e0238339).

RESULTS

Included studies

Of 3 508 studies screened, 31 met the selection and eligibility criteria (Figure 1).

Of these 31 studies (Table 1 and Table 2), 17 (54.8%) were on the first emergence of Ebola virus in 2014, 10 (32.3%) were in Zika virus, three (9.7%) on SARS-CoV-2, and one (3.2%) on H1N1. No studies that matched the inclusion criteria were found for poliovirus. As regards study design, 15 (48.4%) were cross-sectional studies, 12 (38.7%) were ecological studies, three (9.7%) were retrospective cohort studies, and one (3.2%) was a case report.

Ebola virus

Malaria.

During the Ebola virus outbreak in Sierra Leone, there was an increase in malaria self-medication, but not in malaria mortality rates (¹⁸18. Vygen S, Tiffany A, Rull M, Ventura A, Wolz A, Jambai A, et al. Changes in health-seeking behavior did not result in increased all-cause mortality during the Ebola outbreak in Western Area, Sierra Leone. Am J Trop Med Hyg. 2016;95:897–901.). However, in the northern province, discrepancies were seen in mortality notification between regional and national databases, with 66% fewer deaths reported in the national data base. For measles, an opposite trend was seen, with an 80% increase in reported cases of measles in children younger than 5 years (¹⁷17. Sesay T, Denisiuk O, Shringarpure KK, Wurie BS, George P, Sesay MI, et al. Paediatric care in relation to the 2014–2015 Ebola outbreak and general reporting of deaths in Sierra Leone. Public Health Action. 2017;7:S34–9.). Furthermore, consultations for malaria declined by 27% during the Ebola virus outbreak and, in the north, the percentage of patients receiving malaria treatment fell from 75% to 34% (¹⁵15. Moses FL, Tamang D, Denisiuk O, Dumbuya U, Hann K, Zachariah R. Management of malaria in children with fever in rural Sierra Leone in relation to the 2014–2015 Ebola outbreak. Public Health Action. 2017;7:S22–6.). In the south-east of Sierra Leone, similar trends were observed, with a significant reduction in health care being sought for children (¹¹11. Elston JW, Moosa AJ, Moses F, Walker G,Dotta N, Waldman RJ, et al. Impact of the Ebola outbreak on health systems and population health in Sierra Leone. J Public Health (Oxf). 2016;38:673–8.).

In Guinea, the number of children attending health services also dropped significantly (¹²12. Kolie D, Camara BS, Delamou A, Béavogui AH, Hermans V, Edwards JK, et al. The Ebola-effect in Guinea 2014–15: tangled trends of malaria care in children under-five. PLoS One. 2018;13:e0192798., ¹⁶16. Plucinski MM, Guilavogui T, Sidikiba S, Diakité N, Diakité S, Dioubaté M, et al. Effect of the Ebola-virus-disease epidemic on malaria case management in Guinea, 2014: a cross-sectional survey of health facilities. Lancet Infect Dis. 2015;15:1017–1023.). The number of medical consultations decreased as did the number of patients being treated with oral and injectable antimalarial drugs. This affected the frequency of incorrect treatment of negative cases, which decreased from 27% to 19% in the affected areas (¹⁶16. Plucinski MM, Guilavogui T, Sidikiba S, Diakité N, Diakité S, Dioubaté M, et al. Effect of the Ebola-virus-disease epidemic on malaria case management in Guinea, 2014: a cross-sectional survey of health facilities. Lancet Infect Dis. 2015;15:1017–1023.).

In Liberia, access to medical care was hampered, both nationally (¹⁴14. McQuilkin PA, Udhayashankar K, Niescierenko M, Maranda L. Health-care access during the Ebola virus epidemic in Liberia. Am J Trop Med Hyg. 2017;97:931–6.) and in the capital, Monrovia (¹³13. McLean KE, Abramowitz SA, Ball JD, Monger J, Tehoungue K, McKune SL, et al. Community-based reports of morbidity, mortality, and health-seeking behaviours in four Monrovia communities during the West African Ebola epidemic. Glob Public Health. 2018;13:528–44.). Nationally, only 53% (213/401) of patients who sought medical care for malaria received any care (¹⁴14. McQuilkin PA, Udhayashankar K, Niescierenko M, Maranda L. Health-care access during the Ebola virus epidemic in Liberia. Am J Trop Med Hyg. 2017;97:931–6.).

Vaccination.

In Guinea, there was a significant decrease in administration of the following vaccines: yellow fever, measles, tuberculosis, the pentavalent vaccine, and poliomyelitis during the Ebola virus outbreak (²⁰20. Delamou A, Ayadi AME, Sidibe S, Delvaux T, Camara BS, Sandouno SD, et al. Effect of Ebola virus disease on maternal and child health services in Guinea: a retrospective observational cohort study. Lancet Glob Health. 2017;5:e448–57.). Four and ten health centers, respectively, had stock-out problems in the pre-Ebola virus and Ebola virus periods. Vaccine administration declined universally during the outbreak period, with vaccination against tuberculosis (bacillus Calmette–Guérin vaccine) completely stopping. After the Ebola virus outbreak, no vaccine shortages occurred, but overall vaccine administration did not recover to pre-Ebola virus outbreak levels (¹⁹19. Camara BS, Delamou AM, Diro E, El Ayadi A, Béavogui AH, Sidibé S, et al. Influence of the 2014–2015 Ebola outbreak on the vaccination of children in a rural district of Guinea. Public Health Action. 2017;7:161–7.). Furthermore, interruption of stool collection for the diagnosis of poliomyelitis was reported between October 2014 and March 2015 and six cases of circulating vaccine-derived poliovirus type 2 were recorded (²¹21. Fernandez-Garcia MD, Majumdar M, Kebe O, Fall AD, Kone M, Kande M, et al. Emergence of vaccine-derived polioviruses during Ebola virus disease outbreak, Guinea, 2014-2015. Emerg Infect Dis. 2018;24:65–74.).

In Sierra Leone during the Ebola virus outbreak, coverage of the measles vaccine and third dose of the pentavalent vaccine decreased (²³23. Sun X, Samba TT, Yao J, Yin W, Xiao L, Liu F, et al. Impact of the Ebola outbreak on routine immunization in western area, Sierra Leone – a field survey from an Ebola epidemic area. BMC Public Health. 2017;17:363.). In Moyamba district, the average number of children who received all recommended childhood vaccines before the age of 1 year fell by about 50% between the early and late months of 2014 (¹¹11. Elston JW, Moosa AJ, Moses F, Walker G,Dotta N, Waldman RJ, et al. Impact of the Ebola outbreak on health systems and population health in Sierra Leone. J Public Health (Oxf). 2016;38:673–8.). In the prefecture of Lola, suspected measles cases began to appear in January 2015 and reached a peak in April of the same year (²²22. Suk JE, Paez Jimenez A, Kourouma M, Derrough T, Baldé M, Honomou P, et al. Post-Ebola measles outbreak in Lola, Guinea, January–June 2015. Emerg Infect Dis. 2016;22:1106–8.).

HIV/AIDS.

In Sierra Leone, HIV testing decreased but antiretroviral treatment increased unexpectedly (²⁴24. Gamanga AH, Owiti P, Bhat P, Harries AD, Kargbo-Labour I, Koroma M. The Ebola outbreak: effects on HIV reporting, testing and care in Bonthe district, rural Sierra Leone. Public Health Action. 2017;7:S10–5.). Considering data from the 34th Military Hospital in Freetown, which did not suffer structural impacts during the Ebola virus outbreak (for example, stockouts or lack of staff), 83.3% of patients with HIV infection went without treatment for at least 1 day and the risk of missing appointments increased significantly. This situation continued after the end of the Ebola virus outbreak (²⁶26. Nagel E, Blackowicz MJ, Sahr F, Jarrett OD. Impact of the Ebola epidemic on clinical outcomes of HIV-infected soldiers and their dependents in Sierra Leone. Int J STD AIDS. 2019;30:106–12.).

In Guinea, the areas affected by the Ebola virus outbreak saw a significant reduction in the number of pregnant women with HIV infection receiving prenatal care. Furthermore, although the number of pregnant woman with HIV infection did not change, the number of women and children who received antiretroviral treatment to prevent vertical transmission decreased (²⁵25. Leno NN, Delamou A, Koita Y, Diallo TS, Kaba A, Delvaux T, et al. Ebola virus disease outbreak in Guinea: what effects on prevention of mother-to-child transmission of HIV services? Reprod Health. 2018;15:60.).

Tuberculosis.

In Guinea, clinical and bacteriological diagnosis of all forms of tuberculosis fell significantly by 40% corresponding with a sharp drop in notification of cases of tuberculosis in 2014 (²⁷27. Magassouba AS, Diallo BD, Camara LM, Sow K, Camara S, Bah B, et al. Impact of the Ebola virus disease outbreak (2014–2016) on tuberculosis surveillance activities by Guinea’s National Tuberculosis Control Program: a time series analysis. BMC Public Health. 2020;20:1200.). Despite the negative impact of the Ebola virus outbreak on diagnosis and case reporting, the treatment success rate in patients with tuberculosis remained stable at above 80%, with a slight increase after the epidemic (²⁷27. Magassouba AS, Diallo BD, Camara LM, Sow K, Camara S, Bah B, et al. Impact of the Ebola virus disease outbreak (2014–2016) on tuberculosis surveillance activities by Guinea’s National Tuberculosis Control Program: a time series analysis. BMC Public Health. 2020;20:1200.).

ZIKA virus

Neuropathies and congenital malformations.

For the Zika virus outbreak associated with microcephaly, there was an epidemic increase in microcephaly in Brazil and, given lag times, areas with Zika virus clusters became areas of microcephaly clusters over time (³²32. Oliveira WK, de França GVA, Carmo EH, Duncan BB, de Souza Kuchenbecker R, Schmidt MI. Infection-related microcephaly after the 2015 and 2016 Zika virus outbreaks in Brazil: a surveillance-based analysis. Lancet. 2017;390:861–70., ³⁴34. Vissoci JRN, Rocha TAH, Silva NCD, de Sousa Queiroz RC, Thomaz EBAF, Amaral PVM, et al. Zika virus infection and microcephaly: evidence regarding geospatial associations. PLoS Negl Trop Dis. 2018;12:e0006392.). The largest increase in cases of microcephaly was in the north-east of the country, which went from 2.0 cases to 49.9 cases per 10 000 newborns in November 2015 (³²32. Oliveira WK, de França GVA, Carmo EH, Duncan BB, de Souza Kuchenbecker R, Schmidt MI. Infection-related microcephaly after the 2015 and 2016 Zika virus outbreaks in Brazil: a surveillance-based analysis. Lancet. 2017;390:861–70.). During the outbreak, the excess number of hospitalizations for encephalitis, myelitis, and encephalomyelitis in the region reached about 570 (²⁸28. Barcellos C, Xavier DR, Pavão AL, Boccolini CS, Pina MF, Pedroso M, et al. Increased hospitalizations for neuropathies as indicators of Zika virus infection, according to health information system data, Brazil. Emerg Infect Dis. 2016;22:1894–9.).

In Colombia, a record number of microcephaly cases per epidemiological week occurred during the Zika virus epidemic (²⁹29. Mendivelso DFO, García RA, Bedoya RM, Rángel SG. Notificación de defectos congénitos por brote del virus del Zika en Colombia, 2015–2017. Rev Panam Salud Publica. 2019;43:e38., ³⁰30. Hurtado-Villa P, Puerto AK, Victoria S, Gracia G, Guasmayán L, Arce P, et al. Raised frequency of microcephaly related to Zika virus infection in two birth defects surveillance systems in Bogotá and Cali, Colombia. Pediatr Infect Dis. J 2017;36:1017–9.). Nationally, it was estimated that between 10 173.16 and 10 860.57 disability-adjusted life years (DALYs) were lost due to microcephaly caused by Zika-virus (³¹31. Mora-Salamanca AF, Porras-Ramírez A, Restrepo FPH. Burden of disease due to microcephaly associated with the Zika virus in Colombia. Cad Saude Publica. 2020;36:e00215319.).

In the Dominican Republic, a similar pattern was observed, with a peak of Zika virus cases before the peak in microcephaly cases (³³33. Pimentel R, Khosla S, Rondon J, Peña F, Sullivan G, Perez M, et al. Birth defects and long-term neurodevelopmental abnormalities in infants born during the Zika virus epidemic in the Dominican Republic. Ann Glob Health. 2021;87:4.).

Other arboviruses.

Data from the Pan American Health Organization (PAHO) indicate that in Latin America, where dengue cases have been increasing in the past few years, an unusual and significant decline in dengue was seen in several countries by 2016, with a general decline in 2017 and 2018, and a resurgence in 2019. This represents the highest historical peak in several countries, which could indicate a short-lived (12 to 36 months) cross-immunity against dengue as a result of the Zika virus outbreak (³⁶36. Mugabe VA, Borja LS, Cardoso CW, Weaver SC, Reis MG, Kitron U, et al. Changes in the dynamics of dengue incidence in South and Central America are possibly due to cross-population immunity after Zika virus epidemics. Trop Med Int Health. 2021;26:272–80.).

In Brazil, Zika virus affected the series of confirmed and discarded dengue cases and vice versa, suggesting that some discarded and confirmed dengue cases could in fact have been cases of Zika virus infection, and indicating the occurrence of cross-diagnosis and co-infections (³⁷37. Oliveira JF, Rodrigues MS, Skalinski LM, Santos AES, Costa LC, Cardim LL, et al. Interdependence between confirmed and discarded cases of dengue, chikungunya and Zika viruses in Brazil: a multivariate time-series analysis. PLoS One. 2020;15:e0228347.). Similarly, the dengue-endemic area of Cúcuta, Colombia, recorded a drop in dengue notifications during the 2016 Zika virus outbreak (³⁵35. Morgan J, Strode C, Salcedo-Sora JE. Climatic and socio-economic factors supporting the co-circulation of dengue, Zika and chikungunya in three different ecosystems in Colombia. PLoS Negl Trop Dis. 2021;15:e0009259.).

SARS-CoV-2

During the COVID-19 pandemic, sampling, testing, and reporting of poliomyelitis cases by the Global Polio Laboratory Network fell (³⁹39. Zomahoun DJ, Burman AL, Snider CJ, Chauvin C, Gardner T, Lickness JS, et al. Impact of COVID-19 pandemic on global poliovirus surveillance. MMWR 2021;69:1648–52.).

The European Union, which has regularly reported enterovirus outbreaks since 2010, initially experienced a drop in enterovirus D68 notifications at the beginning of the COVID-19 outbreak and then an above-average increase later in the pandemic, precipitated by the widespread relaxation of COVID-19 mitigation measures (³⁸38. Benschop KS, Albert J, Anton A, Andrés C, Aranzamendi M, Armannsdóttir B, et al. Re-emergence of enterovirus D68 in Europe after easing the COVID-19 lockdown, September 2021. Euro Surveill. 2021;26:2100998.).

A similar trend was observed with malaria cases in children younger than 5 years in Sierra Leone. During the lockdown in April 2020, malaria case notifications dropped significantly, and then rose again with the relaxation of distancing measures (⁴⁰40. Buonsenso D, Iodice F, Cinicola B, Raffaelli F, Sowa S, Ricciardi W. Management of malaria in children younger than 5 years old during coronavirus disease 2019 pandemic in Sierra Leone: a lesson learned? Front Pediatr. 2021;8:587638.).

H1N1

Only one article was found on H1N1, based on the European Union early warning and response system. The article reported an historic low in the reporting of non-pandemic events during the increase in H1N1 cases in 2009 (⁴¹41. Cox A, Guglielmetti P, Coulombier D. Assessing the impact of the 2009 H1N1 influenza pandemic on reporting of other threats through the early warning and response system. Euro Surveill. 2009;14:19397.).

Risk of bias assessment

In the quality analysis, two cross-sectional studies had a considerable risk of bias (²²22. Suk JE, Paez Jimenez A, Kourouma M, Derrough T, Baldé M, Honomou P, et al. Post-Ebola measles outbreak in Lola, Guinea, January–June 2015. Emerg Infect Dis. 2016;22:1106–8., ²⁷27. Magassouba AS, Diallo BD, Camara LM, Sow K, Camara S, Bah B, et al. Impact of the Ebola virus disease outbreak (2014–2016) on tuberculosis surveillance activities by Guinea’s National Tuberculosis Control Program: a time series analysis. BMC Public Health. 2020;20:1200.), while nine had a moderate risk of bias (¹¹11. Elston JW, Moosa AJ, Moses F, Walker G,Dotta N, Waldman RJ, et al. Impact of the Ebola outbreak on health systems and population health in Sierra Leone. J Public Health (Oxf). 2016;38:673–8.–¹⁵15. Moses FL, Tamang D, Denisiuk O, Dumbuya U, Hann K, Zachariah R. Management of malaria in children with fever in rural Sierra Leone in relation to the 2014–2015 Ebola outbreak. Public Health Action. 2017;7:S22–6., ¹⁷17. Sesay T, Denisiuk O, Shringarpure KK, Wurie BS, George P, Sesay MI, et al. Paediatric care in relation to the 2014–2015 Ebola outbreak and general reporting of deaths in Sierra Leone. Public Health Action. 2017;7:S34–9., ¹⁸18. Vygen S, Tiffany A, Rull M, Ventura A, Wolz A, Jambai A, et al. Changes in health-seeking behavior did not result in increased all-cause mortality during the Ebola outbreak in Western Area, Sierra Leone. Am J Trop Med Hyg. 2016;95:897–901., ²⁴24. Gamanga AH, Owiti P, Bhat P, Harries AD, Kargbo-Labour I, Koroma M. The Ebola outbreak: effects on HIV reporting, testing and care in Bonthe district, rural Sierra Leone. Public Health Action. 2017;7:S10–5., ³³33. Pimentel R, Khosla S, Rondon J, Peña F, Sullivan G, Perez M, et al. Birth defects and long-term neurodevelopmental abnormalities in infants born during the Zika virus epidemic in the Dominican Republic. Ann Glob Health. 2021;87:4.), and three a low risk (¹⁶16. Plucinski MM, Guilavogui T, Sidikiba S, Diakité N, Diakité S, Dioubaté M, et al. Effect of the Ebola-virus-disease epidemic on malaria case management in Guinea, 2014: a cross-sectional survey of health facilities. Lancet Infect Dis. 2015;15:1017–1023., ²³23. Sun X, Samba TT, Yao J, Yin W, Xiao L, Liu F, et al. Impact of the Ebola outbreak on routine immunization in western area, Sierra Leone – a field survey from an Ebola epidemic area. BMC Public Health. 2017;17:363., ²⁵25. Leno NN, Delamou A, Koita Y, Diallo TS, Kaba A, Delvaux T, et al. Ebola virus disease outbreak in Guinea: what effects on prevention of mother-to-child transmission of HIV services? Reprod Health. 2018;15:60.). Of the cohort studies, two were classified as low risk of bias (²⁰20. Delamou A, Ayadi AME, Sidibe S, Delvaux T, Camara BS, Sandouno SD, et al. Effect of Ebola virus disease on maternal and child health services in Guinea: a retrospective observational cohort study. Lancet Glob Health. 2017;5:e448–57., ²⁶26. Nagel E, Blackowicz MJ, Sahr F, Jarrett OD. Impact of the Ebola epidemic on clinical outcomes of HIV-infected soldiers and their dependents in Sierra Leone. Int J STD AIDS. 2019;30:106–12.) and one as moderate risk (³⁰30. Hurtado-Villa P, Puerto AK, Victoria S, Gracia G, Guasmayán L, Arce P, et al. Raised frequency of microcephaly related to Zika virus infection in two birth defects surveillance systems in Bogotá and Cali, Colombia. Pediatr Infect Dis. J 2017;36:1017–9.). The case study had a moderate risk of bias (²¹21. Fernandez-Garcia MD, Majumdar M, Kebe O, Fall AD, Kone M, Kande M, et al. Emergence of vaccine-derived polioviruses during Ebola virus disease outbreak, Guinea, 2014-2015. Emerg Infect Dis. 2018;24:65–74.).

DISCUSSION

PHEIC are extraordinary events and a considerable challenge for health services (¹1. World Health Organization. International Health Regulations [Internet]. Geneva: WHO 2005 [cited 2022 Apr 27] Available at: https://apps.who.int/iris/bitstream/handle/10665/246107/9789241580496-eng.pdf
https://apps.who.int/iris/bitstream/hand... ). To the best of our knowledge, no other literature reviews have comprehensively assessed the effect of PHEIC on the surveillance and control of notifiable diseases. Their importance comes not only from the possible direct increase in mortality and morbidity in different countries, but also from their secondary impact on local endemic diseases. Several factors influence the performance of health systems and service coverage during PHEIC (³3. Hotez PJ. Neglected tropical diseases in the Ebola-affected countries of West Africa. PLoS Negl Trop Dis. 2015;9:e0003671–⁵5. Effects of the West Africa Ebola virus disease on health-care utilization – A systematic review. Front Public Health. 2016;4:222., ²⁵25. Leno NN, Delamou A, Koita Y, Diallo TS, Kaba A, Delvaux T, et al. Ebola virus disease outbreak in Guinea: what effects on prevention of mother-to-child transmission of HIV services? Reprod Health. 2018;15:60.).

Some health professionals who experienced the Ebola virus outbreak in West Africa in 2014, including in places that were little or not affected by the outbreak, provided explanations for the decrease in health assistance coverage, such as the behavior of the population and dissemination of information. The most common explanations were: patients' fear of contracting Ebola virus disease during the journey to health facilities or within the facilities; distrust of the behavior of health professionals; fear of being sent to Ebola virus disease treatment centers; and the stigma that a positive diagnosis would bring (³3. Hotez PJ. Neglected tropical diseases in the Ebola-affected countries of West Africa. PLoS Negl Trop Dis. 2015;9:e0003671, ⁵5. Effects of the West Africa Ebola virus disease on health-care utilization – A systematic review. Front Public Health. 2016;4:222., ¹¹11. Elston JW, Moosa AJ, Moses F, Walker G,Dotta N, Waldman RJ, et al. Impact of the Ebola outbreak on health systems and population health in Sierra Leone. J Public Health (Oxf). 2016;38:673–8., ¹³13. McLean KE, Abramowitz SA, Ball JD, Monger J, Tehoungue K, McKune SL, et al. Community-based reports of morbidity, mortality, and health-seeking behaviours in four Monrovia communities during the West African Ebola epidemic. Glob Public Health. 2018;13:528–44., ¹⁴14. McQuilkin PA, Udhayashankar K, Niescierenko M, Maranda L. Health-care access during the Ebola virus epidemic in Liberia. Am J Trop Med Hyg. 2017;97:931–6., ¹⁶16. Plucinski MM, Guilavogui T, Sidikiba S, Diakité N, Diakité S, Dioubaté M, et al. Effect of the Ebola-virus-disease epidemic on malaria case management in Guinea, 2014: a cross-sectional survey of health facilities. Lancet Infect Dis. 2015;15:1017–1023., ²⁵25. Leno NN, Delamou A, Koita Y, Diallo TS, Kaba A, Delvaux T, et al. Ebola virus disease outbreak in Guinea: what effects on prevention of mother-to-child transmission of HIV services? Reprod Health. 2018;15:60.).

Other explanations were the limited access to medical care due to the closure of health facilities, denial of care by health professionals, and financial difficulties, given the dependence on out-of-pocket payments for access to health care in sub-Saharan Africa (¹³13. McLean KE, Abramowitz SA, Ball JD, Monger J, Tehoungue K, McKune SL, et al. Community-based reports of morbidity, mortality, and health-seeking behaviours in four Monrovia communities during the West African Ebola epidemic. Glob Public Health. 2018;13:528–44., ¹⁴14. McQuilkin PA, Udhayashankar K, Niescierenko M, Maranda L. Health-care access during the Ebola virus epidemic in Liberia. Am J Trop Med Hyg. 2017;97:931–6.). Among the factors linked to the closing of health facilities was the high mortality in health professionals, which could explain the denial of care, and the low stocks of equipment, medications, and vaccines (⁴4. Parpia AS, Ndeffo-Mbah ML, Wenzel NS, Galvani AP. Effects of response to 2014–2015 Ebola outbreak on deaths from Malaria, HIV/AIDS, and tuberculosis, West Africa. Emerg Infect Dis. 2016;22:433–41., ⁵5. Effects of the West Africa Ebola virus disease on health-care utilization – A systematic review. Front Public Health. 2016;4:222., ¹⁹19. Camara BS, Delamou AM, Diro E, El Ayadi A, Béavogui AH, Sidibé S, et al. Influence of the 2014–2015 Ebola outbreak on the vaccination of children in a rural district of Guinea. Public Health Action. 2017;7:161–7., ²⁵25. Leno NN, Delamou A, Koita Y, Diallo TS, Kaba A, Delvaux T, et al. Ebola virus disease outbreak in Guinea: what effects on prevention of mother-to-child transmission of HIV services? Reprod Health. 2018;15:60.).

Even when services were maintained, sensationalist news played a key role in coverage failure. For example, some women refused HIV testing because of possible Ebola transmission through needles and blood, which increased the number of deliveries that occurred at home and decreased prenatal care. This situation probably increased the HIV viral load of these women, contributing to an increase in mother-to-child transmission, a worsening of their health status, and an increase in HIV transmission to new individuals (¹¹11. Elston JW, Moosa AJ, Moses F, Walker G,Dotta N, Waldman RJ, et al. Impact of the Ebola outbreak on health systems and population health in Sierra Leone. J Public Health (Oxf). 2016;38:673–8., ²⁰20. Delamou A, Ayadi AME, Sidibe S, Delvaux T, Camara BS, Sandouno SD, et al. Effect of Ebola virus disease on maternal and child health services in Guinea: a retrospective observational cohort study. Lancet Glob Health. 2017;5:e448–57., ²⁵25. Leno NN, Delamou A, Koita Y, Diallo TS, Kaba A, Delvaux T, et al. Ebola virus disease outbreak in Guinea: what effects on prevention of mother-to-child transmission of HIV services? Reprod Health. 2018;15:60.).

Such factors were not exclusive to Ebola virus. During the Zika virus epidemic (associated with neuropathies and congenital malformations), other arboviruses were affected. The negative impacts were: misdiagnosis caused by similar symptoms; co-infections; and difficulty in accessing reliable tests. This situation called into question the capacity and reliability of the testing and diagnostic system (³⁵35. Morgan J, Strode C, Salcedo-Sora JE. Climatic and socio-economic factors supporting the co-circulation of dengue, Zika and chikungunya in three different ecosystems in Colombia. PLoS Negl Trop Dis. 2021;15:e0009259., ³⁷37. Oliveira JF, Rodrigues MS, Skalinski LM, Santos AES, Costa LC, Cardim LL, et al. Interdependence between confirmed and discarded cases of dengue, chikungunya and Zika viruses in Brazil: a multivariate time-series analysis. PLoS One. 2020;15:e0228347.). A positive impact of the Zika virus was a possible cross-immunity which led to a decrease in the incidence of dengue immediately after the Zika virus outbreak in some countries (³⁶36. Mugabe VA, Borja LS, Cardoso CW, Weaver SC, Reis MG, Kitron U, et al. Changes in the dynamics of dengue incidence in South and Central America are possibly due to cross-population immunity after Zika virus epidemics. Trop Med Int Health. 2021;26:272–80.).

Furthermore, during the COVID-19 pandemic, testing and diagnosis of poliomyelitis decreased and proper malaria care could not be maintained because of logistic and organizational problems and overload of health systems (³⁸38. Benschop KS, Albert J, Anton A, Andrés C, Aranzamendi M, Armannsdóttir B, et al. Re-emergence of enterovirus D68 in Europe after easing the COVID-19 lockdown, September 2021. Euro Surveill. 2021;26:2100998.–⁴⁰40. Buonsenso D, Iodice F, Cinicola B, Raffaelli F, Sowa S, Ricciardi W. Management of malaria in children younger than 5 years old during coronavirus disease 2019 pandemic in Sierra Leone: a lesson learned? Front Pediatr. 2021;8:587638.).

Understanding these factors is essential for local authorities, as this allows for better crisis management, avoidance or reduction of secondary losses, and possibly a reduction in the direct impact of the emergency itself. For example, the health authorities of Sierra Leone managed to avoid discontinuation of the malaria programs during the COVID-19 pandemic. As a result, only a brief decrease in care occurred during the lockdown, and services soon returned to normal (⁴⁰40. Buonsenso D, Iodice F, Cinicola B, Raffaelli F, Sowa S, Ricciardi W. Management of malaria in children younger than 5 years old during coronavirus disease 2019 pandemic in Sierra Leone: a lesson learned? Front Pediatr. 2021;8:587638.). WHO made available tools to assess the capacity of health facilities to maintain essential health services during the COVID-19 pandemic (⁴²42. World Health Organization. Continuity of essential health services: facility assessment tool: a module from the suite of health service capacity assessments in the context of the COVID-19 pandemic: interim guidance 20 October 2020. Geneva: WHO; 2020 [cited 2022 Sep 29]. Available at: https://apps.who.int/iris/handle/10665/336254
https://apps.who.int/iris/handle/10665/3... ). Authorities in the Americas made appeals for the maintenance of programs on the control and surveillance of infectious diseases, such as dengue (⁴³43. Pan American Health Organization. Epidemiological update dengue in the context of COVID-19. Washington, D.C: PAHO; 2020 [cited 2022 Apr 27]. Available at: https://iris.paho.org/bitstream/handle/10665.2/53174/EpiUpdate3December2020_eng.pdf?sequence=1&isAllowed=y
https://iris.paho.org/bitstream/handle/1... ), Chagas disease (⁴⁴44. Pan American Health Organization. OPAS: 70% das pessoas com Chagas não sabem que estão infectadas [Internet]. Washington, D.C: PAHO; 2020 [cited 2022 Apr 27]. Available at: https://www.paho.org/pt/noticias/13-4-2021-opas-70-das-pessoas-com-chagas-nao-sabem-que-estao-infectadas
https://www.paho.org/pt/noticias/13-4-20... ), malaria (⁴⁵45. Pan American Health Organization. Measures to ensure the continuity of the response to malaria in the Americas during the COVID-19 pandemic, 24 April 2020. Washington, D.C: PAHO; 2020 [cited 2022 Apr 27]. Available at: https://iris.paho.org/handle/10665.2/52080
https://iris.paho.org/handle/10665.2/520... ), and leishmaniasis (⁴⁶46. Pan American Health Organization. Leishmanioses: informe epidemiológico das Américas, No. 10. 2021. Washington, D.C: PAHO; 2021 [cited 2022 Apr 27]. Available at: https://iris.paho.org/handle/10665.2/55386
https://iris.paho.org/handle/10665.2/553... ).

Our results indicate how the weakening of surveillance and control programs during PHEIC can be harmful to the population, sometimes with the indirect effects on other diseases being greater than those directly caused by the emergency.

This review has some limitations and hence the findings should be considered with caution. The increase in notifications in certain emergencies is a possible consequence of a growing of awareness of the disease, leading the population and medical teams to seek a diagnosis. As already mentioned, during the increase in Zika virus infections, some cross-reaction of the dengue and Zika virus tests may have occurred. In addition, the growing concern about the consequences of Zika virus infection in pregnant women led to an increase in the proportion of tests being performed specifically in this group (³⁷37. Oliveira JF, Rodrigues MS, Skalinski LM, Santos AES, Costa LC, Cardim LL, et al. Interdependence between confirmed and discarded cases of dengue, chikungunya and Zika viruses in Brazil: a multivariate time-series analysis. PLoS One. 2020;15:e0228347.). Furthermore, Zika virus notification in Brazil only became compulsory in February 2016. This resulted in biased records of incidence rates in 2015, which could mask the association of Zika virus infection with congenital cases of microcephaly or other diseases (³⁴34. Vissoci JRN, Rocha TAH, Silva NCD, de Sousa Queiroz RC, Thomaz EBAF, Amaral PVM, et al. Zika virus infection and microcephaly: evidence regarding geospatial associations. PLoS Negl Trop Dis. 2018;12:e0006392., ⁴⁷47. Ministério da Saúde. Portaria No - 204, de 17 de fevereiro de 2016 [Internet]. Brasilia: Ministério da Saúde; 2016 [cited 2022 Apr 27]. Available at: https://bvsms.saude.gov.br/bvs/saudelegis/gm/2016/prt0204_17_02_2016.html
https://bvsms.saude.gov.br/bvs/saudelegi... ).

Similarly, the early stages of COVID-19 can easily be confused with dengue, and vice versa, and hence co-infections, cross-reactions, and misdiagnoses in the official prevalence data for both diseases cannot be ruled out. Shared symptoms (such as fever, joint pain, and difficulty breathing) and laboratory parameters (such as lymphopenia, leukopenia, thrombocytopenia, and elevated transaminases) could be confounding factors for diagnosis (⁴⁸48. Suryana K. Coronavirus disease 2019, dengue hemorrhagic fever, and the clinical similarity. Asian J Pharm Clin Res. 2020;9:1–3.).

In addition, even official data could be biased, since most of the diseases are neglected diseases. These diseases mainly affect poor regions of Africa, Asia, and Latin America, and tend to be neglected in terms of resources and medicines available, although greater attention and resources are being given to the “big three diseases” (HIV/AIDS, malaria, and tuberculosis). Thus, it is necessary to consider the possibility that health authorities, especially global authorities, may be unaware of the burden that affects vulnerable populations during outbreaks of PHEIC (⁴⁹49. Chris B, Singh S, Sudarshi D. Neglected tropical diseases, conflict, and the right to health. In: Institute of Medicine (US) Forum on Microbial Threats. The causes and impacts of neglected tropical and zoonotic diseases: opportunities for integrated intervention strategies. Washington, D.C.: National Academies Press (US); 2011 [cited 2022 Apr 27]. Available at: https://www.ncbi.nlm.nih.gov/books/NBK62508/
https://www.ncbi.nlm.nih.gov/books/NBK62... , ⁵⁰50. Atatah PE, Kisavi-Atatah CW. Globalization: revisiting neglected tropical diseases such as malaria and measles. Open J Soc Sci. 2015;3:45–56.). For example, there was a considerable discrepancy between malaria death notifications in regional and national databases in Sierra Leone during the Ebola outbreak (¹⁷17. Sesay T, Denisiuk O, Shringarpure KK, Wurie BS, George P, Sesay MI, et al. Paediatric care in relation to the 2014–2015 Ebola outbreak and general reporting of deaths in Sierra Leone. Public Health Action. 2017;7:S34–9.).

Poliomyelitis and measles are considered by some to be neglected diseases, as they mostly affect the same vulnerable populations and share social and structural characteristics (⁴⁹49. Chris B, Singh S, Sudarshi D. Neglected tropical diseases, conflict, and the right to health. In: Institute of Medicine (US) Forum on Microbial Threats. The causes and impacts of neglected tropical and zoonotic diseases: opportunities for integrated intervention strategies. Washington, D.C.: National Academies Press (US); 2011 [cited 2022 Apr 27]. Available at: https://www.ncbi.nlm.nih.gov/books/NBK62508/
https://www.ncbi.nlm.nih.gov/books/NBK62... , ⁵⁰50. Atatah PE, Kisavi-Atatah CW. Globalization: revisiting neglected tropical diseases such as malaria and measles. Open J Soc Sci. 2015;3:45–56.). The neglected character of poliomyelitis, which is considered to have been eradicated in the Americas, Europe, and South-east Asia through immunizations, may be one of the reasons we found no studies on poliomyelitis for our review.

COVID-19 (2020) and Ebola virus disease (2019) are recent emergencies which may also explain the small number of studies we found, and Ebola virus may have been overlooked because of its overlap with COVID-19. In addition, our search may not have captured all relevant studies, especially in the gray literature.

Conclusions

Factors associated with the effects of PHEIC on notifiable disease surveillance and control programs go beyond health systems and expose socioeconomic inequity as a determinant within affected populations. Despite the undeniable need to control PHEIC as they arise, the diversion of resources and attention from health authorities mainly affects already vulnerable populations. Over time, this can lead to a weakening of health systems, causing the population to lose years of healthy life, and requiring costly future investments. The analysis of these effects is important for the development of new protocols that can better respond to future crises.

Disclaimer.

The authors hold sole responsibility for the views expressed in the manuscript, which may not necessarily reflect the opinion or policy of the Revista Panamericana de Salud Pública / Pan American Journal of Public Health and/or those of the Pan American Health Organization.

Acknowledgements.

GRA and IRA thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the master and doctoral scholarships.

REFERENCES

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