Scoping Review on the Impact of Outbreaks on Sexual and Reproductive Health Services: Proposed Frameworks for Pre-, Intra-, and Postoutbreak Situations
Introduction. Recent experiences from global outbreaks have highlighted the severe disruptions in sexual and reproductive health services that expose women and girls to preventable health risks. Yet, to date, there is no review studying the possible impact of outbreaks on sexual and reproductive health (SRH). Methodology. Studies reporting outbreaks impacting sexual and reproductive health and pregnancy outcomes were identified using MEDLINE, Embase, and ISI-WoS. Reported impacts were reviewed at systems, community, and legislative levels. Results. The initial run listed 4423 studies; the 37 studies that met all inclusion criteria were mainly from Latin America and Africa. Studies on outbreaks of diseases like Zika and Ebola have documented declines in facility-based deliveries, contraceptive use, and antenatal and institutional care due to burdened healthcare system. Service usage was also impacted by a lack of trust in the healthcare system and system shocks, including workforce capacity and availability. At the community level, poverty and lack of awareness were critical contributors to poor access to SRH services. Assessing the target population’s knowledge, attitude, beliefs, and behavior and using health literacy principles for communication were fundamental for designing service delivery. Online resources for SRH services were an acceptable medium of information among young adults. In outbreak situations, SRH and pregnancy outcomes were improved by implementing laboratory surveillance, free-of-cost contraceptive services, improved screening through professional training, and quality of care. In addition, mobile health clinics were reported to be effective in remote areas. Knowledge Contribution. In outbreaks, the interventions are categorized into preoutbreak, during, and postoutbreak periods. The proposed steps can help to improve and do course correction in emergencies. Though conducted before the COVID-19 crisis, the authors believe that lessons can be drawn from the paper to understand and mitigate the impact of the pandemic on sexual and reproductive health services.
In low-resource settings, disease outbreaks have the potential to make health service delivery a challenge. Outbreaks tend to put enormous pressure on the health system to deliver quality healthcare . Poor healthcare quality has been shown to adversely affect health outcomes, especially in low- and middle-income countries . Furthermore, during the outbreak, stressed health systems can be overwhelmed in efforts to provide healthcare to their respective populations due to an increase in demand. In such situations, vulnerable and at-risk population groups such as pregnant mothers and children are especially at greater risk of having adverse health outcomes . It is, therefore, imperative that the impact of outbreaks on sexual and reproductive health (SRH) and pregnancy-related outcomes of vulnerable populations in low-resource settings be further studied for improved response.
Outbreaks are characterized by a localized increase in the number of cases of a particular disease in comparator timeframe . Various social and environmental factors, including overcrowding, armed conflicts, and global warming, drive outbreaks [4, 5]. Outbreaks have the potential to impact SRH and pregnancy-related outcomes [6–10].
Data from 219 countries shows that there has been a significant global rise in outbreaks of human infectious diseases. According to a study, from 1980 to 2013, the number of outbreaks and emerging infectious diseases has increased .
Besides straining healthcare delivery, outbreaks also result in considerable morbidity and mortality, instill widespread fear and social disruptions, and attract large-scale publicity due to their overall damaging effects . For example, during Ebola outbreaks, assessments from West Africa in 2014 showed that lapses in service delivery resulted in the collapse of public trust in health systems . In addition, health system response during outbreaks may be hampered by a low density of human resources for health, low capacity for disease surveillance in the community, infrastructural deficits in health facilities, and weak supply chains for essential medicines .
Adequate outbreak response entails establishing strong linkages between health system resilience, quality of care, and global health security . During outbreaks, the health system challenges can exacerbate health inequalities confronted by at-risk populations not limited to pregnant women and children but for women, girls, adolescents, migrants, refugees, and the poor. Adverse sexual reproductive health and pregnancy outcomes have been observed postsyphilis, Zika, Ebola, and measles infection outbreaks [1, 2, 12]. For example, an impact evaluation of the Ebola outbreak on health systems and population health in Sierra Leone showed a postoutbreak surge in teenage pregnancies. The same study also recorded a reduction in vaccination coverage, highlighting the consequences of outbreaks on fragile health systems, especially in developing countries. Additionally, Zika virus infection is associated with adverse reproductive outcomes that include miscarriage, fetal demise, stillbirth, and congenital malformations such as microcephaly and intrauterine growth restriction .
There is a potential of aggravation in health inequalities confronted by vulnerable segments of the population, such as pregnant women in outbreaks. While Zika infections are associated with adverse reproductive outcomes, it has been observed that even in such situations, the abortion policies remained essentially unchanged . A scoping review of Zika virus literature identified the need for gathering more evidence to improve the understanding of the Zika virus and its impact on public health [14, 15].
1.1. Rationale and Objectives
To inform policy guidance and future planning, there is a need to analyze the literature and evaluate the impact of outbreaks on SRH and pregnancy outcomes. To date, we have not come across any systematic literature review that addresses this topic. This scoping review examines existing evidence on how disease outbreaks lead to adverse SRH outcomes directly or indirectly by impacting health systems, community, and policy response. In addition, we report lessons learned from effective interventions to reduce adverse SRH outcomes before, during, and postoutbreaks and their implications for policymakers.
This scoping review is conducted using Arksey and O’Malley’s methodology and Levac’s methodological enhancement [16, 17]. In addition, the present scoping review has adopted a systematic approach for mapping evidence to identify main concepts on how outbreaks lead to adverse SRH outcomes directly or by impacting health systems, community, and policy response . For the description of the conceptual model used in this scoping review, kindly refer to Figure 1.
2.1. Impact on SRH
(a)Direct effect(b)Indirect effect: depending on the nature of disease and transmission mode, outbreaks affect individual SRH through impacting access and utilization of SRH products and services. This, in turn, through an inadequate health system response, leads to an increase in morbidity and mortality
The burden on a fragile health system increases after an outbreak. Lack of appropriate procedures and guidelines leads to system disruption and collapse, resulting in fewer services (preventive/curative) for patients causing an increase in morbidity and mortality.
2.2. Review Question and Scope
How do outbreaks directly lead to adverse SRH outcomes impacting health systems, community, and policy response? In addition, kindly refer to Table 1 for the key definitions used in this scoping review for developing key concepts.
2.3. Search Strategy
Studies/literature relevant for this scoping review were identified by searching the following electronic databases of the published literature: MEDLINE, Embase, and ISI-WoS (the appendix). These databases cover most of the published peer review on outbreaks and SRH; both being intensely studied topics are unlikely to remain unpublished. Considering the 1994 International Population and Development Conference held in Cairo as a landmark for SRH, we limited our search from January 1995 to August 2018 . Only English articles were considered for this scoping review. The team leader experienced in the literature search in consultation with a librarian identified a draft list of search terms. The WHO technical lead discussed and approved the final set of search terms before running the search. All the records identified through different sources were downloaded in the EndNote library and were screened by two individuals as part of the research team. Studies that report outbreaks having an impact on SRH and pregnancy outcomes were identified.
2.4. Relevance Screening and Inclusion Criteria
Based on the approved protocol, this scoping review consisted of three levels of screening: duplicate removal, title and abstract review, and full-text review.
A screening form was developed before screen abstracts, titles, and keywords of identified citations. EndNote “Find Duplicate” tool was also used to remove duplicates, using author, year title, and volume field matching. A rerun was done by the team leader experienced in literature screening. An eligibility criterion was applied less stringently at this stage to avoid losing any relevant record. Any article that is deemed appropriate for the question of interest is included in the full-text screening stage. In the third level, the team established whether the full-text articles meet the inclusion/exclusion criteria through consultation. Hard to categorize articles were referred to another team member who reviewed and shared his opinion with the team leader, and the decision was made with consensus. An article was of relevance if (a) it is reporting an outbreak (b) concerned with sexual reproductive health and pregnancy outcomes at title abstract/abstract stage. At the full-text screening stage, the article should also be reporting on (c) healthcare service delivery or quality, or (d) access or utilization to healthcare, or (e) health-seeking behavior. The criteria were tested on a sample of abstracts before beginning the abstract review to ensure that they are robust enough to capture any articles with evidence on outbreaks and conditions of interest. Articles from high-income countries (World Bank Classification, World Bank Country and Lending Groups: Country Classification. Available from URL: https://blogs.worldbank.org/opendata/new-country-classifications-income-level-2018-2019, last accessed: Sep 09, 2018.) were excluded as the healthcare systems are often strong enough to bear shocks of outbreaks and do not represent the challenges faced by low- and middle-income countries.
2.5. Study Characterization and Extraction
As described, the team leader developed a data collection instrument to confirm study relevance and extract study characteristics. In addition, the form was pretested by the WHO technical lead before implementation to ensure the data collection instrument is capturing the information accurately.
2.6. Scoping Review Management, Data Charting, and Analysis
The team leader did data abstraction; however, 5% of randomly chosen extracted forms were done by another team member. No significant discrepancies were found, and the data was compiled in a single literature review software program and synthesis and was downloaded into a single Excel spreadsheet in Microsoft Excel software for validation and coding. Following this, the identified quality indicators were extracted and coded.
2.7. Study Contribution
There is a considerable shortage of high-quality published data related to SRH and pregnancies in outbreaks, and evidence is scarce about their background in humanitarian settings. Obstacles include access, cultural and ideological barriers, data challenges, financial and resource constraints, and systemic and sectoral challenges. Higher-quality evidence on SRH and pregnancy-related services in outbreaks through a collective framework is needed to improve access and services. This information is essential for policymakers, donors, and program managers working within SRH in pandemics and outbreaks to making informed decisions at national and global levels.
2.8. Dissemination and Ethics
The results from this scoping review will guide the next phase of a multifaceted research program that will set the direction of further research in the short term and ultimately the development of guidelines that can be implemented at the system level to measure and monitor SRH and pregnancy outcomes during outbreaks. This study did not require ethics approval as it is reviewing data from publicly available materials.
Single-person screening might not be the best way to select studies; however, having an experienced author taking a sensitive approach towards inclusion rather than exclusion reduced possible bias. Excluding non-English language articles would be a major limitation as we might have missed research published in Spanish and French. Nevertheless, if major themes are captured, our objective to guide the future course of action is primarily achieved.
3.1. Scoping Review’s Descriptive Statistics
Using the PRISMA guidelines (as much as applicable for the scoping review), our initial run of the search strategy based on all outbreaks on the WHO webpage list returned 4423 records. After removing 530 duplicate records and 1706 irrelevant diseases (refer to Figure 2), we were left with 2187 records to be screened at the title abstract stage. After removing pre-1995 and ineligible records at the title abstract step, we retrieved full text for 516 records. Out of these, 37 met inclusion criteria and were included in the analysis. Most of the articles were published between 2017 and 2018, with only one in the late 90s. Most of the literature was from Latin America and Africa, with only a handful from Asian countries.
Influenza, Ebola, and Zika were the most frequently studied diseases, followed by meningitis, SARS, and cholera (refer to Table 2).
Most of the studies conducted were at the subnational level; however, studies on national levels were also performed (refer to Tables 3 and 4). Study designs adopted were prospective, retrospective, and cross-sectional. Most studies either focused on SRH or pregnancy outcomes with a few exceptions.
3.2. Thematic Analysis
3.2.1. Health-Related Knowledge, Attitude, and Behavior
Contraceptive commodity sales have been used to indicate healthcare behavior in certain epidemics [24–26]. This is primarily the case with Zika outbreak studies. Therefore, authors have investigated changes in the sales of contraceptives at the country level and pre-, during, and postoutbreak sales. Not much variation has been observed, but very low access to long-acting reversible contraception has been noted .
At subnational-level studies, some have found improved access to and utilization for contraceptive services and improved uptake of most effective methods when provided free of cost . For example, during Zika outbreaks in Brazil, most women wanted to delay pregnancies, but only women with high SES control their intentions . In another study from Brazil, low awareness about contraception was observed, with few women considering a change in pregnancy intentions due to the outbreak . A study on people with disabilities also found low levels of awareness about contraception in South America .
3.2.2. Health System Capacity Building or Readiness
In Brazil, the critical elements to expanding services in SRH and to tackle an outbreak were identified as contraceptive availability, method mix, and utilization pattern which were used as measures of readiness of the health system [32, 33]. During an outbreak, emergency contraceptives were available in almost all pharmacies staffed by pharmacists with a low level of knowledge . Likewise, in Puerto Rico that reported high unintended pregnancies, investigators found a significant unmet need for contraceptives during an outbreak where a large proportion of pregnancies were unintended . A study conducted in an emergency medicine department in Brazil found that a double epidemic of dengue and Zika disrupted routine care . A multicountry study found that the upgradation of ultrasonography services by training for equipment care resulted in improved quality of care .
3.2.3. The Burden of Disease Measurement
Studies assessed the load on health systems in different ways. For example, lab-based surveillance was implemented in Haiti to measure Zika virus disease cases , while in several asymptomatic cases, pregnancy outcomes in Zika and Ebola-infected mothers and trends of incident Zika/Ebola cases have been reported to assess burden on various aspects of the healthcare system [39–41].
3.2.4. Healthcare Service Utilization
Ebola impacted the trust in the healthcare system to provide quality services during outbreaks. Therefore, the most frequently studied aspect was a decline in service utilization. A national-level study for rural settings in Guinea reported a decrease in contraceptive use, antenatal care visits, and institutional deliveries during the Ebola outbreak . However, it also reported postoutbreak recovery of contraception service utilization but not the other two. In several studies, utilization of institutional care, facility-based deliveries, and delay in antenatal visits have been assessed and found to indicate a decline in utilization throughout with little or no recovery in Guinea, Liberia, and Sierra Leone [42–48]. Sierra Leone found that lack of friendly attitude in health facilities and flawed referral system were barriers to facility-based delivery .
3.2.5. Healthcare Service Provision
Triage and isolation protocol implementation and mobile health clinics were found to be effective in Sierra Leone [50, 51]. In addition, despite being at a very high risk of contracting Ebola during the outbreak, nurses and midwives continued to provide care in Sierra Leone due to various motivations, including professional duty, responsibility to the community, and religious beliefs .
3.2.6. The Burden of Disease
A few other studies reported the burden on the disease to indicate the insufficiency or low quality of healthcare service in the wake of an outbreak where lives could have been saved if not the case [53–55]. In Sierra Leone, MNCH services declined due to a weak system, confusion over policy, and the magnitude of the outbreak. Services by CHWs improved with clear instructions despite mistrust by the community. CHWs remained more effective than outsiders .
A study from Turkey reported reduced adverse outcomes by implementing various strategies to handle the pregnant patient load. Strategies included admittance of suspected and confirmed cases to the hospital and testing for potential H1N1 infection . Another study from Brazil observed that pregnant women with influenza consumed a higher amount of healthcare services than their noninfected counterparts, possibly due to a higher death rate .
A study from Haiti reported improved outcomes in low-resource settings among pregnant women with cholera through a women-centered approach of providing obstetric and neonatal services and supervision of hydration status .
A study from Sri Lanka reported an outbreak of fungal meningitis after using improperly stored donated medical supplies during pregnancy and delivery care (including anesthesia medication for cesarean section) after the tsunami highlighting the fact that not only provision of supplies is essential, but these need to be appropriately handled until used .
Scoping reviews are used to map out key concepts behind an area of research. This scoping review analytically reviews the available literature on the impact of outbreaks on SRH and pregnancy outcomes. It reports on the impact of outbreaks on SRH outcomes, whether direct or indirect, affecting health systems, any possible consequences to the community, or policy response. Also reported are the lessons learned from effective interventions aimed at reducing adverse SRH outcomes. The intention is to collate evidence to guide future policy and planning. It is documented that outbreaks are associated with undesirable reproductive health outcomes with no impact on relevant policies, e.g., Zika and Ebola outbreaks . At the time of this review, there was no existing scoping/literature review encompassing this topic. The major infectious diseases causing outbreaks from the pool of the selected studies included influenza (37%), EVD (15%), meningitis (9%), Zika (11%), cholera (6%), and SARS (6%) indicating a range of diseases that can impact SRH among vulnerable populations (Table 3). These diseases have affected the local and global populations and health systems differently.
We report the findings of this review on health system impact in terms of (i) supply-side impact, i.e., services, human resources, and policies; (ii) demand-side impacts, i.e., utilization pattern of SRH services; and (iii) enabling environment, i.e., legislation and policy implications levels.
4.1. Supply-Side Impacts
Exploration of supply-side issues within situational and environmental determinants such as availability and access to modern contraception, vector control, and sociocultural factors related to pregnancy and family planning to prevent diseases like Zika and reproductive health has been emphasized .
The burden on the healthcare system is a primary concern during any outbreak, especially in countries with limited resources. Different studies documenting Zika and Ebola outbreaks resulted in the decline in utilization of services [39–41, 53, 54]. Studies from West African countries like Sierra Leone, Guinea, and Liberia reported poor utilization of institutional care, facility-based deliveries, contraceptive use, and antenatal care during the Ebola outbreak due to overburdened healthcare systems [26, 42–48]. Similarly, inappropriate handling and storage of medical supplies that included anesthesia medication for pregnancy and delivery care, including cesarean surgery, were highlighted in a Sri Lankan study where an outbreak of fungal meningitis among pregnant women was reported posttsunami due to usage of improperly stored medicines .
During the Zika outbreak, few studies reported shortage and stockout of supplies, including contraceptives, availability of trained workforce, method mix, consumption, and access to long-term reversible contraceptive methods [27, 32]. During the Zika outbreak, free-of-cost availability of effective contraception resulted in better use . The knowledge and use were also found low in emergency contraception pills, but they were available in most pharmacies . However, Puerto Rico reported a significant unmet need for contraception, and a considerable proportion of pregnancies were unintended .
Innovative approaches to address the increase in service demands such as triaging patients, implementation of isolation protocols, and use of mobile clinics were effective in Sierra Leone. Personal attributes, including religious beliefs, professional duty, and sense of responsibility to the community of midwives and nurses, also played an essential role in keeping up healthcare services . A study from Turkey reported reduced adverse outcomes due to influenza by implementing multiple strategies, including timely testing and treatment for H1N1 infection .
Another important aspect is that good-quality data on SRH in outbreaks were limited. As a result, there is a lack of evidence of their impact on accessibility and obstacles to using various contraceptive services . Poor healthcare quality adversely affected health outcomes, especially in low- and middle-income countries [63, 64]. This was established in the Ebola outbreak in West Africa in 2014, during which gaps in service delivery combined with lack of public trust in health systems offered challenges to response and recovery .
4.2. Demand-Side Impacts
Reliability and trust in government organizations as a source of information have always been insufficient. This was elicited in a study of college students, which found low use of government websites compared to news media during the Ebola outbreak . Likewise, the Ebola virus disease affected the trust in the healthcare system resulting in a decline in the utilization of services.
Healthcare service utilization was higher among pregnant women suffering from influenza in Brazil than nonpregnant women without the disease .
Few women considered changes in pregnancy intentions during the Zika outbreak due to low awareness regarding contraception in Brazil  and South America . At the same time, there has been minimal variation in sales of contraceptives before, during, and after Zika outbreaks . Other studies report improved access, uptake, and utilization of contraceptive methods at the subnational level . Poverty and lack of awareness were the key determinants to poor utilization of reproductive health services. Sex education, access to contraceptives, safe motherhood, and safe abortion programs should be implemented to prevent discrimination . Another study in Brazil during the Zika outbreak identified relatively low awareness and contraceptive knowledge as the main reason for fewer women changing pregnancy intentions .
Although previous research has shown online sources of information as an acceptable conduit among young adults , including sexual health , simple availability of information is not enough. An exploratory study assessing knowledge, attitude, belief, and behavior regarding reproductive health in the context of Zika reports difficulty in evaluating information and translating it into practice. For example, the behavior change was mainly related to mosquito control rather than the sexual transmission of the disease . Thus, to promote understanding and use of information by the public, there is a need to integrate health literacy and communication principles in disseminating information [68, 69].
4.3. Enabling Environment Impacts
Important risk factors like gender have been identified as missing at the policy level. However, due to differences in exposure level, it needs to be considered during health planning . Different studies have reported novel models to address the outbreak situations. For example, Haiti implemented a policy to strengthen laboratory surveillance to identify Zika cases and measure the burden . A free-of-cost availability of effective contraception resulted in better uptake and utilization during the Zika outbreak in Puerto Rico . During the EVD outbreak in Sierra Leone, policies to improve screening accuracy, nursing skills, IPC, and quality of care resulted in increased efficiency and quality of system depicted by the enhanced patient flow . Similarly, the communities received mobile health clinics in Sierra Leone enthusiastically, particularly in remote areas .
Implementation of a surveillance system was also identified as an integral model which, through appropriate legislation, can be a valuable tool to counter outbreaks and their impact on SRH. For example, complex monitoring of Zika, including laboratories, vector control, social mobilization, and clinical care, was successful during the Zika outbreak in Haiti [33, 38]. Lack of availability of abortion guidelines also was noted in Brazil during the Zika outbreak . Another study in Guatemala, El Salvador, Dominican Republic, Honduras, and Haiti emphasized the need for upgradation of diagnostic services in the context of the Zika virus epidemic . In addition, there is a large gap between the demand and availability of contraception in Puerto Rico. In the backdrop of many unintended pregnancies, there was a need to improve availability and access to contraception through legislation or policy , which needs appropriate action from the highest level.
Renewed focus on global health protection has been demonstrated by establishing weaknesses in public health preparedness by outbreaks like Zika and Ebola . The International Health Regulations (IHR) was updated in 2007, keeping outbreaks like Ebola and Zika. The aim was to prevent, protect, control, and provide public health response to the international spread of diseases. The broader scope of these regulations was to advocate for urgent action and strengthen national systems and infrastructure . Quality FP services (known as QFP) were set as the standard of care for family planning to help reproductive-age men and women accomplish their desired spacing and healthy children .
There is significant evidence of vulnerable populations being at greater risk, primarily because of outbreaks like Zika, Ebola, and measles [73, 74]. Hence, there is a need to improve health literacy efforts that recognize risk perceptions as barriers to behavior change. Use of health literacy principles such as using local lay-man language should be part of such health communication messages targeted at establishing a connection between reproductive health and diseases like Zika and adopting the information for behavior change among reproductive-age men and women . In addition, further research on information-seeking behavior as to where people could go for information and where they go for information can be helpful to identify areas of improvement .
The United Nations also responded to pandemics by developing guidelines and frameworks to strengthen public health response and strengthen national systems. In response to Zika, the UN created a Global Strategic Response Framework and Joint Operational Plan, which had six pillars, namely, (i) surveillance, (ii) community engagement and risk communication, (iii) vector control and personal protection, (iv) care for those affected, (v) research, and (vi) coordination. The International Medical Advisory Panel (IMAP) also prepared a statement approved by the International Planned Parenthood Federation (IPPF) for member states to ensure that sexual and reproductive health rights of women and couples are adequately protected . This statement complements WHO’s information and other guidelines [77–79]; in addition, WHO has published a framework designing sexual health programs that identify multisectoral approaches . All these are helpful tools for national governments to adopt and utilize for developing and implementing legislation as per their needs and resources.
As this scoping review was conducted before the present pandemic COVID-19 emerged, the authors strongly believe that the lessons can also be drawn from this paper to understand and mitigate the impact of the pandemic on sexual and reproductive health services. Historically it is evident that restriction in movement and lockdown leads to confining individuals, couples, and families, leading to spending more time at home with the possibility of increased unprotected sexual activity . In addition, multiple lockdowns will lead to home isolation due to the fears of contracting the virus, which can lead to a decrease in uptake of SRH services and increase in reported cases of intimate partner violence, and some geographies will reduce access to contraception and safe abortion care including in vulnerable populations and refugees . It is also likely that stockouts of easily accessible short-term methods of contraception such as condoms or oral pills can happen due to global chain disruption. Thus, some estimates suggest that this pandemic will lead to higher rates of unintended pregnancy, unsafe abortion, short interpregnancy intervals, and untreated sexually transmitted infections .
4.4. Proposed Framework for Outbreaks
The World Health Organization has defined an outbreak as “a disease outbreak is the occurrence of disease cases more than normal expectancy. Several cases vary according to the disease-causing agent, and the size and type of previous and existing exposure to the agent” (https://www.who.int/environmental_health_emergencies/natural_events/en/).
Based not only on the findings emerging from this scoping review but also in the light of relevant literature on frameworks developed by a different organization such as WHO and UNFPA during various outbreaks in consultation with partners and stakeholders, the authors, therefore, are proposing a framework to identify and understand the prevailing gaps about SRH and pregnancy outcomes in the context of infectious disease-related outbreaks. It is also helpful for plugging these identified gaps with locally acceptable measures that can effectively address the needs of high-risk populations. This comprehensive framework can be used in different settings and can be modified based on locally acceptable and adoptable measures.
The proposed framework (refer to Figure 3) is divided into the following three components based on the timing of an outbreak: (1)Preoutbreak(2)During the outbreak(3)Postoutbreak
Each component deals with issues prevailing during a particular stage of an outbreak. This framework can also address prevailing gaps about any type of outbreak and is not specific to a disease. Components relevant to SRH are described here; for details on the complete framework, refer to Figure 3.
(A)Surveillance (a)Surveillance and monitoring (i)Implement a sensitive surveillance system(ii)Use of digital technology for communication, awareness generation, and education(b)Diagnostic services (i)Establish a laboratory network(c)Case response(B)Sexual and reproductive health services (a)Sexual education(b)Prevention and control of HIV/STIs(c)Antenatal, intrapartum, and postnatal care(d)Contraception provision(e)Fertility care(f)Safe abortion services(C)Legislation (a)Human rights-based approaches (i)Address all aspects such as equality, availability, and quality(b)Cultural values(c)Women empowerment
4.4.2. During Outbreak
(A)Response (a)Engage communities (i)Engage communities through risk communication, engagement, and capacity building(ii)Promote the use of digital technology for communication(b)Control (i)Vector control through PPE and improved SRH services(c)Guidelines (i)Develop patient care guidelines and protocols(d)Enhanced surveillance(e)Diagnostic testing(f)Treatment(B)Sexual and reproductive health services(a)Sexual health (i)Comprehensive education and information(ii)Gender-based violence prevention, support, and care(iii)Prevention and control of HIV and other sexually transmissible infections(iv)Sexual function and psychosexual counseling(b)Reproductive Health(i)Antenatal, intrapartum, and postnatal care(ii)Contraception counseling and provision(iii)Fertility care(iv)Safe abortion care
(A)Surveillance (a)Maintain a sensitive surveillance system(b)Use of digital technology for communication, awareness generation, and education(B)Research (a)Public health research(b)Product development(C)Legislation (a)Policy development and upgradation(b)Legislation for research and development
The current lack of high-quality published data related to SRH and pregnancies in an outbreak situation; the scarcity of evidence about their background in humanitarian settings, especially its accessibility; and the obstacles to using various contraceptive services raise critical concerns. Higher-quality evidence on SRH and pregnancy-related services in outbreaks are needed to improve access to SRH in outbreaks, including voluntary family planning and safe abortion services. Hence, providing greater access to rights-based equitable family planning services, addressing the use of equality could substantially contribute to achieving the SDG goals during an outbreak, especially in a global crisis at scale.
Recent outbreaks of Ebola virus disease, Zika virus disease, SARS, Middle East respiratory syndrome, and influenza H1N1 exposed high maternal morbidity and mortality rates, fetal loss, and fetal harm. As countries maintain or adjust public health measures, emergency legislation, and economic policies in response to the outbreak situations, especially the recent COVID-19 pandemic, there is an urgent need to protect the rights of and support the most vulnerable members of society. This information is essential for policymakers, donors, and program managers working within the area of SRH in outbreaks or crisis-like situations to make informed decisions regarding sustaining SRH interventions aimed at continuation of family planning use, safe abortion care, pregnancy-related services, and PAC indicators at respective national and global levels.
It is the responsibility of governments to respond at local and national levels, and the health officials are also required to provide leadership for health systems . Before making any decision, the policymakers must factor in the direct effects and the indirect effects of the outbreaks. For example, the 2014 Ebola virus outbreak in West Africa showed that the indirect effects of the outbreak were more severe than the outbreak itself . Based on the limited availability of dedicated frameworks on SRH and pregnancies in an outbreak situation, our review attempts to bridge the knowledge gaps through collating lessons learned derived from effective interventions to reduce adverse SRH outcomes before, during, and postoutbreaks and their implications for policymakers. The decisions taken by any government in responding to an outbreak will have consequences for the health and livelihoods of populations. In the context of these decisions, our review highlights the need to consider how to mitigate the effect of system-level disruptions and the decline in service uptake, including facility-based deliveries, contraceptive use, and antenatal and institutional care during an outbreak especially in countries with limited resources. In addition, to expedite the community- and policy-level response to the poor access issue of SRH services, the review suggested implementing gender-specific, equity-based awareness-raising interventions as key increase access and utilization of SRH services. Therefore, our analysis provides “pre-, during, and postoutbreak period” frameworks that policymakers can use to prioritize interventions and quantify the effects to inform decisions around health system continuity and the stopgap measures during and following the outbreak. In the future, it will be worthwhile to conduct a metanalysis for possible variations owing to sociodemographic indicators such as income, age, and education of the cases in the studies included in this scoping review of the available literature impacting knowledge, access, and utilization of services during a pandemic.
Outbreaks are not only public health emergencies, but they can also turn into political and socioeconomic emergencies. The lessons learned from African Ebola and cholera responses taught us to avoid the tunnel vision approach and actively address broader socioeconomic and health inequities when designing measures to counter the emergencies [83, 84]. The results will guide the next phase of a multifaceted research program that will guide further research and development of guidelines that can be implemented at the system level to measure and monitor SRH and pregnancy outcomes during outbreaks and pandemic situations.
A.1. MEDLINE Search Strategy (as of Jul 3, 2018)
(1)exp CHIKUNGUNYA FEVER/or Chikungunya.mp.(2)Cholera.mp. orexp CHOLERA/(3)exp Hemorrhagic Fever, Crimean/or Crimean-Congo hemorrhagic fever.mp.(4)Hendra virus infection.mp. OrexpHenipavirus Infections/(5)Influenza.mp. orexp Influenza, Human/(6)Lassa fever.mp. orexp Lassa Fever/(7)Marburg virus disease.mp. orexp Marburg Virus Disease/(8)Meningitis.mp. orexp MENINGITIS/(9)MERS-CoV.mp. orexp Middle East Respiratory Syndrome Coronavirus/(10)exp MONKEYPOX/or Monkeypox.mp.(11)Nipah virus infection.mp. orexpHenipavirus Infections/(12)exp PLAGUE/ or Plague.mp.(13)Rift Valley fever.mp. orexp Rift Valley Fever/(14)exp severe acute respiratory syndrome/or SARS.mp.(15)Smallpox.mp. orexp SMALLPOX/(16)exp Tularemia/or Tularaemia.mp.(17)Yellow fever.mp. orexp Yellow Fever/(18)Yellow fever.mp. orexp Yellow Fever/(19)expZika Virus Infection/ or expZika Virus/or zika.mp.(20)exp Ebolavirus/ or exp Hemorrhagic Fever, Ebola/or Ebola.mp.(21)1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 or 9 or 10 or 11 or 12 or 13 or 14 or 15 or 16 or 17 or 18 or 19 or 20(22)birth control.mp. orexp Contraception/(23)family planning.mp. orexp Family Planning Services/(24)Contraceptive services.mp.(25)exp Abortion, Induced/ or exp Abortion, Spontaneous/or abortion.mp.(26)pregnancy termination.mp.(27)exp Cesarean Section/or c-section.mp. or c section.mp. or cesarean.mp.(28)prenatal.mp. orexp Prenatal Care/or antenatal.mp.(29)pregnancy complications.mp. orexp pregnancy Complications/(30)delivery.mp. orexp Delivery, Obstetric/(31)(post-natal or postnatal or post-natal or ((post or post-) and care)).mp.(32)(post-abortion care or post-abortion care or postabortion care).mp.(33)exp Reproductive Health Services/or Reproductive health service.mp.(34)or/22-33(35)epx disease outbreaks/or epidemic.mp.(36)21 and 34 and 35(37)limit 36 to ed=19950101-20180531
A.2. Embase Search Strategy (as of Jul 3, 2018)
A closely matching search strategy was run for Embase with exact date limits.
A.3. ISI Web of Science
Diseases: CHIKUNGUNYA FEVER or Cholera or Hemorrhagic Fever or Crimean or Hendra virus infection or Influenza or Lassa fever or Marburg virus disease or Meningitis or MERS-CoV or MONKEYPOX or Nipah virus infection or PLAGUE or Rift Valley fever or severe acute respiratory syndrome or Smallpox or Tularemia or Yellow fever or yellow fever or Zika Virus Infection or Ebolavirus
Reproductive health services: birth control or Contraception or family planning or Family Planning Services or Contraceptive services or Abortion, Induced or Abortion, Spontaneous or abortion or pregnancy termination or Cesarean Section or c-section or c section or cesarean or prenatal or Prenatal Care or antenatal or pregnancy complications or Pregnancy Complications or delivery or Delivery, Obstetric or (post-natal or post-natal or post-natal or ((post or post-) and care)) or (post-abortion care or post-abortion care or post-abortion care) or Reproductive Health Services or Reproductive health service
Epidemic: Disease outbreak or Epidemic
Date limit: Jan 01, 1995, to Jul 3, 2018 (as no more precise date restriction applicable)
It is a scoping review type of a review article where peer reviewed journal articles were used in the literature review are available from open sources such as MEDLINE, EMBASE and ISI-WoS.
Conflicts of Interest
The authors declare that they have no conflicts of interest.
Large anonymous donor funded the study under Grant ID 5149 for women, communities, and health systems in the context of Zika.
World Health Organization, Organisation for Economic Co-operation and Development, The World Bank, Delivering quality health services: a global imperative for universal health coverage, Geneva, 2018, http://apps.who.int/iris/bitstream/handle/10665/272465/9789241513906-eng.pdf?ua=1.
J. W. Elston, A. J. Moosa, F. Moses et al., “Impact of the Ebola outbreak on health systems and population health in Sierra Leone,” Journal of Public Health (Oxford, England), vol. 38, no. 4, pp. 673–678, 2016.View at: Google Scholar
Association IE, A Dictionary of Epidemiology, Oxford University Press, New York, USA, 4th edition, 2001.
C. Caminade, K. M. McIntyre, and A. E. Jones, “Impact of recent and future climate change on vector-borne diseases,” Annals of the New York Academy of Sciences, vol. 1436, no. 1, p. 157, 2018.View at: Google Scholar
K. Letendre, C. L. Fincher, and R. Thornhill, “Does infectious disease cause global variation in the frequency of intrastate armed conflict and civil war?” Biological Reviews of the Cambridge Philosophical Society, vol. 85, no. 3, pp. 669–683, 2010.View at: Publisher Site | Google Scholar
A. T. Boyd, S. T. Cookson, M. Anderson et al., “Centers for Disease Control and Prevention public health response to humanitarian emergencies, 2007-2016,” Emerging infectious diseases, vol. 23, no. 13, 2017.View at: Google Scholar
R. J. Brennan and R. Nandy, “Complex humanitarian emergencies: a major global health challenge,” Emergency Medicine, vol. 13, no. 2, pp. 147–156, 2001.View at: Publisher Site | Google Scholar
S. L. Sharara and S. S. Kanj, “War and infectious diseases: challenges of the Syrian civil war,” PLoS Pathogens, vol. 10, no. 11, article e1004438, 2014.View at: Publisher Site | Google Scholar
K. F. Smith, M. Goldberg, S. Rosenthal et al., “Global rise in human infectious disease outbreaks,” J R Soc Interface, vol. 11, no. 101, article 20140950, 2014.View at: Publisher Site | Google Scholar
M. J. Toole and R. J. Waldman, “Refugees and displaced persons. War, hunger, and public health,” Journal of the American Medical Association, vol. 270, no. 5, pp. 600–605, 1993.View at: Publisher Site | Google Scholar
E. V. Velényi, “World Scientific Handbook of global health economics and public policy. 1, The economics of health and health systems,” in World Scientific Series in Global Healthcare Economics and Public Policy. 1, R. M. Scheffler, Ed., p. 572, World Scientific Publishing (Imperial College Press), London, UK, 2016.View at: Google Scholar
A. C. Tricco, E. Lillie, W. Zarin et al., “PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation,” Annals of Internal Medicine, vol. 169, no. 7, pp. 467–473, 2018.View at: Publisher Site | Google Scholar
M. Carabali, N. Austin, N. B. King, and J. S. Kaufman, “The Zika epidemic and abortion in Latin America: a scoping review,” Global health research and policy, vol. 3, no. 1, p. 15, 2018.View at: Publisher Site | Google Scholar
L. A. Waddell and J. D. Greig, “Scoping review of the Zika virus literature,” PLoS One, vol. 11, no. 5, article e0156376, 2016.View at: Publisher Site | Google Scholar
M. N. Nkangu, O. A. Olatunde, and S. Yaya, “The perspective of gender on the Ebola virus using a risk management and population health framework: a scoping review,” Infectious Diseases of Poverty, vol. 6, no. 1, p. 135, 2017.View at: Publisher Site | Google Scholar
A. Hilary and O. M. Lisa, “Scoping studies: towards a methodological framework,” International journal of social research methodology, vol. 8, no. 1, pp. 19–32, 2005.View at: Google Scholar
D. Levac, H. Colquhoun, and K. K. O'Brien, “Scoping studies: advancing the methodology,” Implementation Science, vol. 5, no. 1, p. 69, 2010.View at: Publisher Site | Google Scholar
WHO, What is quality of care and why is it important? 2018, http://www.who.int/maternal_child_adolescent/topics/quality-of-care/definition/en/.
World Health Organization, Delivering Quality Health Services A Global Imperative for Universal Health Coverage, OECD Publishing, Geneva, 2018.
D. B. Evans, J. Hsu, and T. Boerma, “Universal health coverage and universal access,” The Bulletin of the World Health Organization, vol. 91, no. 8, pp. 546–546A, 2013.View at: Publisher Site | Google Scholar
WHO, Glossary of terms and tools, 2018, http://www.who.int/gender-equity-rights/knowledge/glossary/en/.
J. A. Hall, L. Benton, A. Copas, and J. Stephenson, “Pregnancy intention and pregnancy outcome: systematic review and meta-analysis,” Maternal and Child Health Journal, vol. 21, no. 3, pp. 670–704, 2017.View at: Publisher Site | Google Scholar
UN, Cairo Declaration on Population & Development, ICPPD, 1994, https://www.un.org/popin/icpd/conference/bkg/egypt.
M. Ali and L. Bahamondes, “Contraceptive sales in the setting of the Zika virus epidemic,” European Journal of Contraception and Reproductive Health Care, vol. 23, Supplement 1, p. 126, 2018.View at: Google Scholar
L. Bahamondes, M. Ali, I. Monteiro, and A. Fernandes, “Contraceptive sales in the setting of the Zika virus epidemic,” Human reproduction, vol. 32, no. 1, pp. 88–93, 2017.View at: Google Scholar
B. S. Camara, A. Delamou, E. Diro et al., “Effect of the 2014/2015 Ebola outbreak on reproductive health services in a rural district of Guinea: an ecological study,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 111, no. 1, pp. 22–29, 2017.View at: Publisher Site | Google Scholar
M. Ali, “WHOs response to Zika virus epidemic and assessment of contraceptive sales in affected areas,” European Journal of Contraception and Reproductive Health Care, vol. 23, Supplement 1, p. 15, 2018.View at: Google Scholar
E. Lathrop, L. Romero, S. Hurst et al., “The Zika Contraception Access Network: a feasibility programme to increase access to contraception in Puerto Rico during the 2016-17 Zika virus outbreak,” Lancet Public Health, vol. 3, no. 2, pp. E91–e99, 2018.View at: Publisher Site | Google Scholar
L. J. Marteleto, A. Weitzman, R. Z. Coutinho, and S. V. Alves, “Women's reproductive intentions and behaviors during the Zika epidemic in Brazil,” Population and Development Review, vol. 43, no. 2, pp. 199–227, 2017.View at: Publisher Site | Google Scholar
A. L. V. Borges, C. Moreau, A. Burke, O. A. D. Santos, and C. B. Chofakian, “Women's reproductive health knowledge, attitudes and practices in relation to the Zika virus outbreak in northeast Brazil,” PLoS One, vol. 13, no. 1, article e0190024, 2018.View at: Publisher Site | Google Scholar
M. Roa, “Zika virus outbreak: reproductive health and rights in Latin America,” The Lancet, vol. 387, no. 10021, p. 843, 2016.View at: Publisher Site | Google Scholar
M. Ali, R. Folz, K. Miller, B. R. Johnson Jr., and J. Kiarie, “A study protocol for facility assessment and follow-up evaluations of the barriers to access, availability, utilization and readiness of contraception, abortion and postabortion services in Zika affected areas,” Reproductive health, vol. 14, no. 1, p. 18, 2017.View at: Publisher Site | Google Scholar
M. Ali and A. Tavares, “Assessment of health system readiness in the provision of contraception and abortion/post-abortion services in Zika affected areas in Brazil,” European Journal of Contraception and Reproductive Health Care, vol. 23, Supplement 1, p. 140, 2018.View at: Google Scholar
M. P. Tavares and A. M. Foster, “Emergency contraception in a public health emergency: exploring pharmacy availability in Brazil,” Contraception, vol. 94, no. 2, pp. 109–114, 2016.View at: Publisher Site | Google Scholar
N. K. Tepper, H. I. Goldberg, M. I. Bernal et al., “Estimating contraceptive needs and increasing access to contraception in response to the Zika virus disease outbreak--Puerto Rico, 2016,” MMWR Morbidity and mortality weekly report, vol. 65, no. 12, pp. 311–314, 2016.View at: Publisher Site | Google Scholar
S. N. Fonseca, L. H. Sigaki, A. Teixeira et al., “Enduring a dengue/zika epidemic in Ribeirao Preto, Brazil,” American Journal of Tropical Medicine and Hygiene, vol. 95, 5 Supplement 1, p. 39, 2016.View at: Google Scholar
B. Kallam, A. Abuhamad, J. Hermida et al., “Development of obstetric ultrasound service delivery assessment tools in the context of the Zika virus epidemic in five USAID priority countries,” American Journal of Obstetrics and Gynecology, vol. 217, no. 6, pp. 724-725, 2017.View at: Publisher Site | Google Scholar
I. Journel, L. L. Andrécy, D. Metellus et al., “Transmission of Zika Virus — Haiti, October 12, 2015-September 10, 2016,” MMWR Morbidity and mortality weekly report, vol. 66, no. 6, pp. 172–176, 2017.View at: Publisher Site | Google Scholar
M. Besnard, D. Eyrolle-Guignot, P. Guillemette-Artur et al., “Congenital cerebral malformations and dysfunction in fetuses and newborns following the 2013 to 2014 Zika virus epidemic in French Polynesia,” Eurosurveillance, vol. 21, no. 13, 2016.View at: Publisher Site | Google Scholar
M. C. Castro, Q. C. Han, L. R. Carvalho, C. G. Victora, and G. V. A. Franca, “Implications of Zika virus and congenital Zika syndrome for the number of live births in Brazil,” Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 24, pp. 6177–6182, 2018.View at: Publisher Site | Google Scholar
C. Flamand, C. Fritzell, S. Matheus et al., “The proportion of asymptomatic infections and spectrum of disease among pregnant women infected by Zika virus: systematic monitoring in French Guiana, 2016,” Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin, vol. 22, no. 44, 2017.View at: Google Scholar
K. J. Brolin Ribacke, A. J. van Duinen, H. Nordenstedt et al., “The impact of the West Africa Ebola outbreak on obstetric health care in Sierra Leone,” PLoS One, vol. 11, no. 2, article e0150080, 2016.View at: Publisher Site | Google Scholar
Y. Hyjazi, J. Aribot, R. Waxman, T. Pleah, and B. Dao, “The impact of the Ebola virus epidemic on reproductive and maternal health care services in Guinea,” International Journal of Gynecology & Obstetrics, vol. 131, SUPPL. 5, pp. E156–E1E7, 2015.View at: Google Scholar
N. N. Leno, A. Delamou, Y. Koita et al., “Ebola virus disease outbreak in Guinea: what effects on prevention of mother-to-child transmission of HIV services?” Reproductive Health, vol. 15, no. 1, p. 60, 2018.View at: Publisher Site | Google Scholar
J. R. Lori, S. D. Rominski, J. E. Perosky et al., “A case series study on the effect of Ebola on facility-based deliveries in rural Liberia,” BMC Pregnancy and Childbirth, vol. 15, no. 1, p. ???, 2015.View at: Publisher Site | Google Scholar
I. N. Luginaah, J. Kangmennaang, M. Fallah, B. Dahn, F. Kateh, and T. Nyenswah, “Timing and utilization of antenatal care services in Liberia: understanding the pre-Ebola epidemic context,” Social science & medicine (1982), vol. 160, pp. 75–86, 2016.View at: Publisher Site | Google Scholar
J. Ly, V. Sathananthan, T. Griffiths et al., “Facility-based delivery during the Ebola virus disease epidemic in rural Liberia: analysis from a cross-sectional, population-based household survey,” PLoS medicine, vol. 13, no. 8, article e1002096, 2016.View at: Publisher Site | Google Scholar
A. Delamou, A. M. El Ayadi, S. Sidibe et al., “Effect of Ebola virus disease on maternal and child health services in Guinea: a retrospective observational cohort study,” The Lancet Global health, vol. 5, no. 4, pp. e448–e457, 2017.View at: Publisher Site | Google Scholar
S. Theuring, A. P. Koroma, and G. Harms, ““In the hospital, there will be nobody to pamper me”: a qualitative assessment on barriers to facility-based delivery in post-Ebola Sierra Leone,” Reproductive Health, vol. 15, no. 1, p. 155, 2018.View at: Publisher Site | Google Scholar
D. L. Garde, A. M. R. Hall, R. H. Marsh, K. P. Barron, K. L. Dierberg, and A. P. Koroma, “Implementation of the first dedicated Ebola screening and isolation for maternity patients in Sierra Leone,” Annals of Global Health, vol. 82, no. 3, p. 418, 2018.View at: Google Scholar
R. E. Guetiya Wadoum, A. Samin, N. G. Mafopa et al., “Mobile health clinic for the medical management of clinical sequelae experienced by survivors of the 2013-2016 Ebola virus disease outbreak in Sierra Leone, West Africa,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 36, no. 11, pp. 2193–2200, 2017.View at: Publisher Site | Google Scholar
S. Jones, B. Sam, F. Bull et al., “Even when you are afraid, you stay: provision of maternity care during the Ebola virus epidemic: a qualitative study,” Midwifery, vol. 52, pp. 19–26, 2017.View at: Publisher Site | Google Scholar
L. M. Bebell, T. Oduyebo, and L. E. Riley, “Ebola virus disease and pregnancy: a review of the current knowledge of Ebola virus pathogenesis, maternal, and neonatal outcomes,” Birth defects research, vol. 109, no. 5, pp. 353–362, 2017.View at: Publisher Site | Google Scholar
P. C. Henwood, L. M. Bebell, R. Roshania et al., “Ebola virus disease and pregnancy: a retrospective cohort study of patients managed at 5 Ebola treatment units in West Africa,” Clinical infectious diseases: an official publication of the Infectious Diseases Society of America, vol. 65, no. 2, pp. 292–299, 2017.View at: Publisher Site | Google Scholar
K. Mupapa, W. Mukundu, M. A. Bwaka et al., “Ebola hemorrhagic fever and pregnancy,” The Journal of infectious diseases, vol. 179, Suppl 1, pp. S11–S12, 1999.View at: Publisher Site | Google Scholar
N. P. Miller, P. Milsom, G. Johnson et al., “Community health workers during the Ebola outbreak in Guinea, Liberia, and Sierra Leone,” Journal of global health, vol. 8, 2018.View at: Google Scholar
H. G. Kanmaz, S. S. Oguz, O. Erdeve et al., “Dealing with pandemic influenza A during postpartum and early neonatal period in a busy family-centered neonatal intensive care unit,” The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians, vol. 24, no. 6, pp. 804–807, 2011.View at: Publisher Site | Google Scholar
A. A. da Silva, T. M. S. Ranieri, F. D. Torres et al., “Impact on pregnancies in south Brazil from the influenza A (H1N1) pandemic: cohort study,” PloS one, vol. 9, no. 2, article e88624, 2014.View at: Publisher Site | Google Scholar
I. Ciglenecki, M. Bichet, J. Tena et al., “Cholera in pregnancy: outcomes from a specialized cholera treatment unit for pregnant women in Léogâne, Haiti,” PLoS neglected tropical diseases, vol. 7, no. 8, article e2368, 2013.View at: Publisher Site | Google Scholar
P. S. Gunaratne, C. N. Wijeyaratne, P. Chandrasiri et al., “An outbreak of Aspergillus meningitis following spinal anaesthesia for caesarean section in Sri Lanka: a post-tsunami effect?” The Ceylon medical journal, vol. 51, no. 4, pp. 137–142, 2006.View at: Publisher Site | Google Scholar
J. J. Rasanathan, S. MacCarthy, D. Diniz, E. Torreele, and S. Gruskin, “Engaging human rights in the response to the evolving Zika virus epidemic,” American Journal of Public Health, vol. 107, no. 4, pp. 525–531, 2017.View at: Publisher Site | Google Scholar
K. Blanchet, A. Ramesh, S. Frison et al., “Evidence on public health interventions in humanitarian crises,” Lancet, vol. 390, no. 10109, pp. 2287–2296, 2017.View at: Publisher Site | Google Scholar
J. W. Peabody, M. M. Taguiwalo, D. A. Robalino et al., “Improving the Quality of Care in Developing Countries,” in Disease Control Priorities in Developing Countries. 2nd edition, D. T. Jamison, J. G. Breman, A. R. Measham et al., Eds., The International Bank for Reconstruction and Development / The World Bank, Washington (DC), 2006, https://www.ncbi.nlm.nih.gov/books/NBK11790/.View at: Google Scholar
Data for measuring health care quality and outcomes, OECD Health Care Quality Indicators Project Paris: Organisation for Economic Cooperation and Development, http://www.oecd.org/els/health-systems/health-care-qualityindicators.htm.
T. Koralek, M. G. Runnerstrom, B. J. Brown, C. Uchegbu, and T. B. Basta, “Lessons from Ebola: sources of outbreak information and the associated impact on UC Irvine and Ohio University college students,” PLoS currents, vol. 8, 2016.View at: Publisher Site | Google Scholar
R. Briones, “Harnessing the web: how e-health and e-health literacy impact young adults’ perceptions of online health information,” Medicine 2.0, vol. 4, no. 2, p. e5, 2015.View at: Google Scholar
E. R. Buhi, E. M. Daley, H. J. Fuhrmann, and S. A. Smith, “An observational study of how young people search for online sexual health information,” Journal of American College Health, vol. 58, no. 2, pp. 101–111, 2009.View at: Publisher Site | Google Scholar
E. L. Thompson, C. A. Vamos, L. G. Liggett, S. B. Griner, and E. M. Daley, “Using a health literacy analytic framework to explore Zika virus and reproductive health,” Health Literacy Research and Practice, vol. 2, no. 2, 2018.View at: Google Scholar
K. Parson, M. P. Allen, W. Alvarado-Little, and R. Rudd, Health literacy insights for health crises, 2017, https://nam.edu/health-literacy-insights-for-health-crises.
V. J. Dzau and P. Sands, “Beyond the Ebola Battle — Winning the war against future epidemics,” The New England Journal of Medicine, vol. 375, no. 3, pp. 203-204, 2016.View at: Publisher Site | Google Scholar
R. W. Glynn and M. Boland, “Ebola, Zika and the International Health Regulations – implications for port health preparedness,” Globalization and Health, vol. 12, no. 1, p. 74, 2016.View at: Publisher Site | Google Scholar
L. Gavin, S. Moskosky, M. Carter et al., “Providing quality family planning services recommendations of CDC and the U.S. Office of Population Affairs,” Morbidity and Mortality Weekly Report: Recommendations and Reports, vol. 63, no. 4, 2014.View at: Google Scholar
E. C. Chibueze, V. Tirado, K. D. Lopes et al., “Zika virus infection in pregnancy: a systematic review of disease course and complications,” Reproductive Health, vol. 14, no. 1, p. 28, 2017.View at: Publisher Site | Google Scholar
L. Newman, M. Kamb, S. Hawkes et al., “Global estimates of syphilis in pregnancy and associated adverse outcomes: analysis of multinational antenatal surveillance data,” PLoS Medicine, vol. 10, no. 2, article e1001396, 2013.View at: Publisher Site | Google Scholar
A. G. Brega, M. A. Freedman, L. B. WG et al., “Using the health literacy universal precautions toolkit to improve the quality of patient materials,” Journal of Health Communication, vol. 20, Suppl. 2, pp. s69–s76, 2015.View at: Google Scholar
IMAP, Statement on Zika virus and sexual and reproductive health, 2016.
World Health Organization, Women in the Context of Microcephaly and Zika Virus Disease. Online Q&A, 2016, http://www.who.int/features/qa/zika-pregnancy/en/.
World Health Organization, Zika Virus Disease: Questions and Answers. Online Q&A, 2016, http://www.who.int/features/qa/zika/en/.
World Health Organization, Zika Virus. Factsheet, 2016, http://www.who.int/mediacentre/factsheets/zika/en/.
World Health Organization, Sexual health and its linkages to reproductive health: an operational approach, World Health Organization, Geneva, 2017, License: CC BY-NC-SA 3.0 IGO.
V. Sharma, D. De Beni, A. Sachs Robertson, and F. Maurizio, “Why the promotion of family planning makes more sense now than ever before?” Journal of Health Management, vol. 22, no. 2, pp. 206–214, 2020.View at: Publisher Site | Google Scholar
T. Riley, E. Sully, Z. Ahmed, and A. Biddlecom, “Estimates of the potential impact of the COVID-19 pandemic on sexual and reproductive health in low- and middle-income countries,” International Perspectives on Sexual and Reproductive Health, vol. 46, pp. 73–76, 2020.View at: Publisher Site | Google Scholar
E. T. Richardson, M. B. Barrie, J. D. Kelly, Y. Dibba, S. Koedoyoma, and P. E. Farmer, “Biosocial approaches to the 2013–2016 Ebola pandemic,” Health and Human Rights, vol. 18, no. 1, pp. 115–128, 2016.View at: Google Scholar
S. Chigudu, The Political Life of an Epidemic: Cholera, Crisis, and Citizenship in Zimbabwe, Cambridge University Press, Cambridge, 2020.