Next Article in Journal
Arbovirus and Its Potential to Lead the Next Global Pandemic from Sub-Saharan Africa: What Lessons Have We Learned from COVID-19?
Previous Article in Journal
Monitoring SARS CoV-2 Antibodies Positivity in Healthcare Workers After Inactivated CoronaVac® Vaccine
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Germs
Volume 12
Issue 4
10.18683/germs.2022.1357
germs-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
Germs is published by MDPI from Volume 15 Issue 4 (2025). Previous articles were published by another publisher in Open Access under a CC-BY (or CC-BY-NC-ND) licence, and they are hosted by MDPI on mdpi.com as a courtesy and upon agreement with the former publisher Infection Science Forum.
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Zika Virus: An Opportunity to Revisit Reproductive Health Needs and Disparities

by
Richard A. Stein
1,*,
Alexis Grayon
1,
Adi Katz
2 and
Frank A. Chervenak
2
1
Tandon School of Engineering, Department of Chemical and Biomolecular Engineering, 6 MetroTech Center, Brooklyn, NY 11201, USA
2
Department of Obstetrics and Gynecology, Lenox Hill Hospital, Donald and Barbara Zucker School of Medicine at Hofstra Northwell, 110 E 77th Street, New York, NY 10075, USA
*
Author to whom correspondence should be addressed.
Germs 2022, 12(4), 519-537; https://doi.org/10.18683/germs.2022.1357
Submission received: 30 August 2022 / Revised: 24 October 2022 / Accepted: 29 December 2022 / Published: 31 December 2022
Versions Notes

Abstract

First isolated in 1947, the Zika virus was initially connected only to limited or sporadic human infections. In late 2015, the temporal clustering of a Zika outbreak and microcephaly in newborn babies from northeastern Brazil, and the identification of a causal link between the two, led to the characterization of the congenital Zika syndrome. In the wake of the epidemic, several countries from Latin America advised women to postpone pregnancies for periods ranging from six months to two years. These recommendations initiated critical conversations about the challenges of implementing them in societies with limited access to contraception, widespread socioeconomic inequalities, and high rates of unplanned and adolescent pregnancies. The messaging targeted exclusively women, despite a high prevalence of imbalances in the relationship power, and addressed all women as a group, failing to recognize that the decision to postpone pregnancies will impact different women in different ways, depending on their age at the time. Finally, in several countries affected by the Zika epidemic, due to restrictive reproductive policies, legally terminating a pregnancy is no longer an option even at the earliest time when brain malformations as part of the congenital Zika syndrome can be detected by ultrasonography. The virus continued to circulate after 2016 in several countries. Climate change models predict an expansion of the geographical area where local Zika transmission may occur, indicating that the interface between the virus, teratogenesis, and reproductive rights is a topic of considerable interest for medicine, social sciences, and public health for years to come.

Introduction

The Zika virus is an emerging arthropod-borne virus or arbovirus [1,2] that belongs to the genus Flavivirus from the family Flaviviridae [3]. The virus was first isolated in 1947 from a febrile rhesus macaque monkey in the Zika Forest from Uganda, and while there is some controversy about the first time when it was isolated from humans, this appears to have been in 1964 in Uganda [4,5,6,7,8,9,10]. For over half a century, the Zika virus only caused limited or sporadic human infections in Africa and Asia until the 2007 outbreak from Yap Island in Micronesia, the western Pacific [6,11]. Only 14 cases of Zika virus disease were documented worldwide before this outbreak [12]. During the 2007 outbreak, it was estimated that 73% of the residents three years and older on the island became infected [11]. This was followed by an October 2013 outbreak in the French Polynesia, which extended until April 2014 and from where the virus spread, around the same time, to Easter Island, where it caused a 2014 outbreak, and to the Americas [13,14,15].
In May 2015, the local transmission of Zika was reported in the Americas for the first time, when the virus emerged in northern Brazil [7,16,17]. Based on phylogenetic analyses and molecular clock studies, it was estimated that the virus was introduced to the Americas in the second half of 2013 [18]. By the time it was recognized that the virus may cause severe congenital disease, it has already spread from Brazil to >40 countries [19]. Local mosquito-borne transmission of the Zika virus in the US was first reported in December 2015 in Puerto Rico [20]. In the continental US, the first instance of local transmission was reported in July 2016 in Florida [21] and then in November 2016, in Texas [22]. The sequencing of Zika viruses isolated from patients and infected mosquitoes showed that the virus was introduced into Florida on multiple independent occasions, at least four, but possibly as many as 40, and that probably its local transmission began in the spring of 2016, months before the virus was first detected [23]. The World Health Organization (WHO) declared the Zika virus epidemic a Public Health Emergency of International Concern (PHEIC) on February 1, 2016 [24,25] and, as of July 2019, 87 countries or territories reported local transmission [26,27,28,29]. Viral genomics and travel surveillance found that an outbreak occurred in Cuba in 2017, at a time when circulation of the virus was already waning in other places in the Americas [19]. After the period of Public Health Emergency of International Concern ended in November 2016, >100,000 cases of Zika virus infection were reported in Brazil [30] and >150,000 cases were reported in the Americas by the end of September 2021 [30]. The virus was detected in other locations that include Mexico [31], Gabon [32], India [33,34,35], Papua New Guinea [36], and countries in the Caribbean [37]. The first laboratory-confirmed case of Zika in India was confirmed in November 2016 [38] and the virus was still circulating in several states in India in 2021 [33,35,39]. Some of the historical milestones of the Zika virus emergence and spread are presented in Table 1.
The Zika virus can be transmitted to humans by infected mosquitoes [40], sexually by infected male or female partners [41], perinatally [42], by blood transfusion [43,44], through laboratory exposure [45], or as a result of organ transplantation [46]. Even though the virus was detected in breast milk, its transmission through breastfeeding was not yet documented as of 2021 [47,48,49].

The congenital Zika syndrome

Until October 2015, Zika was generally considered a benign disease [47]. In adults, the Zika virus infection is symptomatic in approximately 20-25% of the infected individuals and causes a mild and usually self-limiting flu-like illness [50] lasting for 7-10 days, usually without long-term consequences [6,51]. However, it was also linked to subcutaneous bleeding [50], cardiovascular changes such as myocarditis, heart failure, and arrhythmia [52,53,54], conjunctivitis, uveitis [55], arthralgia [52], Guillain-Barré syndrome, and meningoencephalitis [56].
In October 2015, reports from northeastern Brazil revealed an increase in the number of babies born with microcephaly and this, together with their temporal clustering, led to the hypothesis that microcephaly was caused by the Zika virus [57]. Because historically the Zika virus was not linked to birth defects, and due to disparities in the incidence of microcephaly in different geographical locations, the initial increase in microcephaly cases was thought to be caused by environmental chemicals [58,59]. Subsequently, several studies provided epidemiological evidence that linked Zika virus exposure during pregnancy to microcephaly [60,61,62,63]. An analysis that used data collected from the Brazilian Information System on Live Births (SINASC) showed that between 2000, prior to the circulation of the virus, and 2015, there was a 9.8-fold increase in the annual average number of microcephaly cases [64].
The virus was isolated from the brain of infants with microcephaly who died, and from the placenta of women who had miscarriages and suspected Zika infections [50]. In a pregnant woman who was infected in week 11 of her pregnancy, the fetal head circumference percentile decreased between week 16 and week 20 from the 47th to the 24th percentile. After her pregnancy was terminated at 21 weeks, viral-like particles were isolated from the fetal brain, and Zika virus replication was detected in a cell culture inoculated with the fetal brain sample [65]. A study that followed another woman, who was infected during her first trimester, documented progressive changes in the fetus upon imaging, and later in the newborn, including ventriculomegaly, cerebral calcifications, and a reduction in the head circumference [66]. A 2016 case report described a pregnant woman who learned after a 29-week ultrasonography about the presence of fetal microcephaly together with fetal and placental calcifications, and after her pregnancy was terminated, fetal autopsy showed that the Zika virus was present in the fetal brain, and the complete viral genome was recovered [67]. The viral genome was also detected in the amniotic fluid of two women whose fetuses presented microcephaly, a finding that strengthened this connection and confirmed the ability of the virus to cross the placenta [68]. It was suggested that the Hofbauer cells of the placenta, which are large vacuolated placental macrophages that appear on day 18 of the pregnancy [69,70,71], may play a role in the transmission of the virus to the fetal brain [72]. Collaborative, multi-disciplinary approaches were critical in causally linking Zika virus to microcephaly [58,73,74,75].
It was estimated that the risk of microcephaly was about 1-13% for infections that occurred during the first trimester of the pregnancy [76,77]. In an observational analysis of >4 million births from Brazil, the relative risk to develop microcephaly with structural changes in the brain was on average 16.80 if infection happened during the first two trimesters of pregnancy [78]. It was shown that the substitution of a single serine to asparagine in prM, one of the three structural proteins of the Zika virus, increased its infectivity in human and murine neural progenitor cells, the severity of the microcephaly in mice, and mortality in newborn mice. Phylogenetic and molecular clock analyses revealed that this mutation emerged for the first time in May 2013, just months prior to the outbreak in French Polynesia, and was maintained subsequently as the virus spread to the Americas [79].
Zika virus infection during pregnancy led to fetal manifestations that extended beyond microcephaly [80] and included growth restriction [81], cerebellar hypoplasia [82], calcification of the subcortical region and basal nuclei [83,84], ventriculomegaly [66], decreased brain volume [84,85], and fetal death [60]. The Zika virus emerges as the newest member of the TORCH pathogens, and the most teratogenic window for Zika is the first trimester of pregnancy [77,86]. Based on the association between Zika virus infection and the multiple serious congenital manifestations, it was recommended that TORCH be renamed TORCHZ [66] or TORZiCH [87].

Family planning recommendation in the wake of the Zika epidemic

On November 11, 2015, the Brazilian Ministry of Health recognized the Zika virus outbreak as a national public health emergency [88,89]. In January 2016, the health ministries from several countries issued advisories for women to postpone pregnancies by 6 months to 2 years [90]. Countries where such recommendations were made include Jamaica [51,91,92,93], Panama [93], Colombia [51,93,94,95], Brazil [51,94,95], El Salvador [51,93,94,95,96], and Ecuador [51,94,95]. Subsequently, in June 2016, the World Health Organization recommended individuals of reproductive age, residing in areas that had local Zika transmission, to be correctly informed and oriented to consider delaying pregnancy, but the language about delaying pregnancies was later removed in an updated guidance in September of the same year [97,98,99,100]. In this context, the epidemic reignited discussions about family planning [101,102], contraception [103], and safe abortion [104,105,106,107].

Criticism of the family planning recommendations

Advisories that recommended women to avoid or postpone pregnancies in the wake of the Zika epidemic have been extensively criticized for several reasons. In all the countries that issued these advisories, close to half or sometimes over half of the pregnancies are unintended [90,108,109,110,111,112], sometimes with marked within-country variations [113]. Up to 50% of the women from Latin American countries give birth for the first time in adolescence [114] and 15-19-year-old adolescents from Latin America and the Caribbean account for 16% of the fertility among women of reproductive age, the highest rate worldwide [115]. Moreover, conversations about sexuality and family planning are considered a cultural taboo in several countries that were affected by the outbreak [114,116,117,118,119]. While the use of modern contraceptives in Latin America increased in recent decades, several gaps persist, and these include high out-of-pocket costs [120]; disparities for marginalized groups [121], indigenous women, those from rural areas, and poor populations [122]; and a slow uptake of long-acting reversible contraception methods [123]. Poor access to healthcare in general, and particularly to reproductive healthcare, creates major barriers in the ability of women to utilize family planning services [51,101,103,124,125,126,127]. Burke and Moreau describe an overlap between areas where the risk of Zika virus infection is highest and those where the access to reproductive and family planning is most restrictive [101].
Socioeconomic inequalities, prevalent in Latin America [122,128,129], and also pervasive in the US [125,130,131], additionally restrict access to reproductive health services. In most countries where the recommendations were issued, the most impoverished women have the lowest access to antenatal care [132]. This becomes even more relevant, considering that the risk of unintended pregnancies is higher among impoverished communities [133,134,135], and minorities, poor, and pregnant women are more susceptible to vector-borne diseases [103,136,137,138,139]. Velez and Diniz refer to the inequalities in sexual and reproductive health as a hidden pandemic: hidden because it is largely ignored, and pandemic because it impacts subgroups of women in a generalized manner [96].
Hodge et al. point out that recommendations to avoid or postpone pregnancies are not purposeful if access to contraception, prenatal care, and safe abortions are not provided [95]. However, 95% of women from Latin America live in a country where access to abortion is legally restricted [140], and even in countries where it is legal, many women face barriers in safely accessing the services [141,142,143]. After a total ban on abortions was instituted in El Salvador in 1997, a constitutional amendment passed in 1999 defined life as beginning at the moment of conception [144]. In El Salvador abortion is considered, without exception, a criminal offence [96], it is not allowed even for victims of rape or incest, or when the woman’s life is in danger and, based on this law, women have been prosecuted and convicted with prison sentences of up to 40 years [144,145,146,147]. Analyses of newspaper articles and court documents found that many of the women convicted of reproduction-related “crimes” had in fact stillbirths that occurred late in pregnancy [144]. In July 2017, a 19-year-old woman who became pregnant as a result of rape and delivered a stillborn baby received a 30-year prison sentence under an “aggravated homicide” charge [147]. She was subsequently acquitted in 2019 after a new trial [148,149]. In another example, a 21-year-old woman with systemic lupus erythematosus, pre-eclampsia, and renal failure, whose fetus presented anencephaly, had to wait for over a month before learning that the Salvadorian Supreme Court denied her petition to have an abortion in 2013. The doctors eventually performed a premature induction of birth via hysterotomy at 27 weeks of gestation. The newborn died and the mother survived, and anti-abortion advocates pointed out that this example illustrates that an abortion is not necessary to save a pregnant woman’s life [150,151]. In Colombia, abortion has become available for all women infected with Zika [152,153], but it was reported that this was not widely publicized [107].
Another shortcoming of the recommendations made in the wake of the Zika epidemic was that with the exception of the WHO advisory, which also included men [154], advisories issued early on were generally directed at women and inherently placed on them the entire burden and responsibility for delaying pregnancies. In a study of items from public health communication campaigns that intended to raise awareness about the Zika virus in Brazil, Coutinho et al. found that the messages on avoiding the mosquito vector and preventing the disease largely excluded men, reinforcing traditional gender roles [155]. Osamor and Grady relevantly point out that most attention in the wake of the Zika outbreak was directed at mosquito control, the pregnant population, and the summer Olympics, but largely omitted the role of men in behaviors related to viral transmission [156]. Even though both men and women are involved in reproductive decisions, family planning has historically focused on women [157], and major gaps persist in incorporating male reproductive responsibilities into initiatives that target reproduction [158]. An analysis of media coverage related to Zika in 186 articles published in two major Brazilian newspapers revealed two sub-frames of the dominant “war” against the virus. One of them supported vector eradication, and the other one emphasized the need to control microcephaly, but placed the burden of prevention on women [159]. Efforts to include men in reproductive health decisions have increased in recent years, but much improvement in the gender-inclusive family planning programs is still needed [160].
The almost exclusive focus on women, as part of recommendations to delay pregnancies, becomes even more disconcerting considering that some of the countries where this recommendation was made overlap with the ones marked by a prevalent and pervading lack of power balance in the sexual relationship, and where sexual assault, violence between partners, and rape are common [137,161,162]. Velez and Diniz note that women affected by the Zika crisis live in asymmetrical power relationships and cannot freely make decisions about their bodies [96]. In many Latin American countries, as a result of the machismo-marianismo gender constructs, with males and females assuming more dominant and submissive gender ideals, respectively, females become more vulnerable to adverse sexual and reproductive health outcomes [163,164,165]. Referring to recommendations made by various countries affected by the epidemic, the UN pointed out that they fail to acknowledge that many women and girls simply cannot exercise control over whether or when or under what circumstances they become pregnant [166]. Wenham et al. underscore the absence of gender in the policy response to an epidemic in which the gender dimensions were very obvious from early on and highlight that without including women’s voices in the arbovirus control plans, the sustainability of this intervention could be questionable [167].
In a survey of women from Fortaleza, Brazil, who were using exclusively the national public health care system, Stolow et al. found that participants perceived the recommendations about postponing pregnancies to be against their cultural norms and did not consider Zika as a reason to use contraception, except for women who self-identified as more affluent. This emphasized that recommendations to postpone pregnancies failed to adequately take social norms into consideration [168].
The recommendation that women postpone pregnancies was criticized for another flaw. As Luna notes, the message addressed women as a group, but failed to take into consideration that during a woman’s reproductive lifespan, a two-year delay of a pregnancy may have very different implications depending on the age group, and while it may be feasible for young women, it may hinder the ability of older women to ever have biological children [146].

Zika and reproductive behaviors and outcomes

Various studies showed that women’s reproductive behavior in response to the Zika outbreak changed in multiple and complex ways. Rangel et al. found a ~25% decline in the size of birth cohorts in Brazil ~18 months after the risk of viral infection peaked. The magnitude of this decline was larger than the one caused by other events that impacted pregnancies, such as the economic conditions during the 2008 recession from the US. Changes in reproductive behavior were larger for more educated and for older women [169].
Using focus group data, Marteleto et al. found that during the first 18 months of the epidemic from Brazil, many women did not want to be pregnant but older women, many of them of higher socioeconomic status, and who had not yet achieved their desired family size, were an exception. Measures to minimize the risk of infection included attempting to conceive during the winter months, using mosquito repellent, living in neighborhoods with a low mosquito prevalence, and wearing long-sleeve shirts. Women of low socioeconomic status identified multiple obstacles in their ability to access contraception. Even though all participants expressed a willingness to seek abortion had they become infected, those of lower socioeconomic status reported predominantly having access to medical abortion, while those of higher socioeconomic status, to a combination of medical and surgical approaches. This highlighted that women of lower socioeconomic status were more likely to carry to term a pregnancy affected by the virus [170].
An analysis of data from the non-profit organization Women on Web (WoW), an online platform available in five languages that operates worldwide and provides access to abortion medication in countries where this is not available safely [171], found that after November 2015, when the Pan American Health Organization issued a Zika virus alert, the number of requests for abortion medication from several Latin American countries increased significantly, and more than doubled in Brazil and Ecuador. Almost half of the women accessing the services in Brazil were poor and younger than 25 years old [172,173,174]. In Brazil, abortion is allowed only in cases of rape, for pregnancies that pose a significant risk to the woman’s life, and in cases of fetal anencephaly [175,176,177,178].

The Zika virus and implications in the changing reproductive climate from the US

Anencephaly can be reliably diagnosed on ultrasound around weeks 10 to 14 of the pregnancy [179,180], and microcephaly is usually recognized only later [181]. During the Zika epidemic, the WHO recommended a fetal anomaly scan between weeks 18 and 20 of gestation or as early as possible after 20 weeks [182]. In several countries, and in about half the US states, where the access to abortion was severely curtailed after the June 24, 2022 reversal of the Roe v. Wade 1973 landmark precedent [183], and abortion is expected to become largely illegal [184], the pregnant population will have limited options, which include continuing a pregnancy with a severely affected fetus, or seeking reproductive care in other states or countries. As of mid-2022, several states in the US banned abortions either in almost all instances, except for when it is required to save the life of the pregnant person, or after six weeks of pregnancy, with civil or criminal penalties for violating the respective laws, and more states are expected to implement restrictions in the near future [185,186,187]. As a result of these and similar restrictions, at the time when anencephaly or microcephaly can be detected on ultrasound, terminating a pregnancy will already be prohibited by law in many US states [188,189,190,191].
The two main mosquito vectors that can transmit the Zika virus in the US are Aedes (Stegomyia) aegypti (L.) and Aedes (Stegomyia) albopictus (Skuse) [192]. Ae aegypti, which most likely originated from Africa [193] and was first reported in the continental US in 1828 [194], is most abundant in the southeastern and southwestern US states [195,196]. Ae. albopictus originated in Asia, it was first detected in the continental US in 1985 [197], where it was probably introduced through the used tire trade [198], and it was in addition found in several northeastern and northwestern states and along the Pacific coast [196,199,200]. Between 1995 and 2016, Ae. albopictus and Ae. aegypti were reported in 40 and in 28 US states and the DC, respectively [192,201] and, in 2016, local Zika transmission in the US was reported in Florida and Texas [202,203]. Were the Zika virus to return to the US, several states that could see local transmission, based on the distribution of the mosquito vectors, are among the most restrictive ones with respect to the access to abortion services [98].
It is expected that Zika virus outbreaks may occur in the future in various countries, partly as a result of the warming climate [204]. An analysis that used existing data to model the transmission dynamics of the Zika virus between humans and vectors, and accounted for seasonal temperature variations, identified temperature as a dominant driver of the basic reproduction number and of the size of the epidemic. The model predicted that even though transmission would not occur when the temperature is constant at 23°C, which is representative of the annual average conditions in Rio de Janeiro, Brazil, it may nevertheless occur in locations with a mean temperature of 20°C if 10°C seasonal variations were present, which is close to the conditions that exist in Tampa, FL. These findings underscored the importance of incorporating climate change dynamics into prospective models, and the possibility that Zika outbreaks may impact broader areas than the ones predicted by static models [205]. In another climate change modeling study, Ryan et al. anticipated that >1.3 billion new people will likely be at risk for Zika virus by 2050 [206]. The potential re-emergence of the Zika virus in previously affected locations, and its emergence in new geographical areas, continue to be of worldwide concern for several reasons, including the implications for reproductive health and rights.

Parallels with rubella

A virus causing congenital abnormalities to the extent of Zika was not seen since the rubella outbreaks in the 1950s [207,208]. Rubella was recognized as early as 1814 as a benign infectious disease characterized by rash, adenopathy, and fever [209]. In 1941 Sir Norman McAlister Gregg, an Australian ophthalmologist, reported that congenital cataracts and heart malformations were more frequent in the offspring of mothers who had rubella during pregnancy [210], and subsequently added deafness as an additional manifestation [211], defining what became known as the classic triad of the congenital rubella syndrome (CRS) [209,212,213,214]. Infection can be associated with other complications, such as microcephaly, bone and dental lesions, cerebral calcifications, and hypospadias [215]. The rubella virus was the first teratogenic virus described [216] and it is the most teratogenic virus currently known [217] and, just like the Zika virus and two other TORCH pathogens, cytomegalovirus and Toxoplasma gondii, was also associated with congenital microcephaly [218,219]. The first trimester and the early second trimester of the pregnancy are the most vulnerable in terms of developing CRS, and it develops in almost all fetuses if infection happens before 8 weeks of gestation [220]. Between 1964 and 1965, 12.5 million cases of rubella were documented in the US, and led to >11,000 therapeutic abortions or miscarriages and the birth of >20,000 infants with CRS [221]. An estimated 100,000 or more cases of CRS still occur globally every year, making it a global public health concern [222,223,224]. The rubella epidemic from 1964-1965 is one of the events credited with reforming abortion law in the US [225,226].

Zika virus at the convergence of multiple disparities

The Zika virus epidemic disproportionately impacted marginalized and impoverished women, and it further accentuated disparities [146,155,227]. Nearly 39% of the Zika virus infections in Mexico occurred in the four states with the highest unmet need for contraception, where disparities in family planning and the ones to mosquito-borne diseases were shown to overlap. A criticism of the approach adopted by the Mexican government in the wake of the Zika outbreak is that it mirrored the approach used for other infectious diseases transmitted by Aedes mosquitoes, such as dengue and chikungunya, and the fact that, even though ~42% of the confirmed Zika cases occurred in women, the focus was placed on mosquito control but not on counseling about contraception. In the US, the geographical regions most likely to experience local Zika transmission overlap with the ones that have the highest rates of unintended pregnancies and where accessing contraception is most challenging [103]. Nearly 10 million US women live in a contraception desert [228,229], which is defined as a county where less than one clinic exists for every 10,000 women who need publicly funded contraception [230], and many groups, including minorities, low-income individuals, and those from rural areas, face large differences in their ability to access contraception [228,231,232].
A study that enrolled 54 women who had children with confirmed or suspected congenital Zika syndrome, living in Alagoas, a state in northeastern Brazil with one of the highest rates of adolescent pregnancies, found that the outbreak initiated and accentuated inequalities that have existed in the country even before the epidemic. For example, 76% of the women did not return to work after the birth of their child, 55% of them depended on transportation provided by their municipality to take their infant to therapy sessions, and 53% of the families did not have resources to purchase prescription medication to control seizures [233].
A Supreme Court case in Brazil, initially filed in 2016 to request protection for women and children affected by Zika, and scheduled for April 2020, was dismissed in the wake of the COVID-19 pandemic. The fact that women lived through two major public health crises, each of them disproportionately affecting minorities and poor populations [233,234], accentuated the disparities and vulnerabilities that they faced [227,233,235].
Wenham et al. point out that, for multiple reasons, the social and economic impact of Zika, COVID-19, and other infectious disease outbreaks predominantly affected women. These include the fact that women are disproportionately affected by decreased access to reproductive health services, have more responsibilities as caretakers, and are more frequently the victims of domestic violence [236].

The interface between a teratogenic mosquito-borne virus and reproductive rights

The rubella epidemic catalyzed biomedical advances and social reforms that played important roles during the Zika virus outbreak. At the interface between a vector-borne teratogenic virus and reproductive rights, Zika is uniquely positioned to guide the management of other emerging and re-emerging infectious diseases with teratogenic potential.
When the Zika virus outbreak peaked in 2016 in the Americas, local transmission was reported in 87 countries and territories from tropical and subtropical regions [28]. The possibility that the virus will spread to more countries and/or that it will reemerge in places with prior transmission is an important consideration [237,238]. The framework to address the impact of the Zika virus should extend beyond classic healthcare interventions such as vector control and improving living conditions. It needs to empower women of reproductive age and their families [239], incorporate sexual and reproductive rights [240], and account for structural inequalities that permeate healthcare [241].
The authors are concerned with recent developments in the United States and several other countries that have eroded women’s reproductive options [242,243,244,245]. We strongly support the autonomy of pregnancy capable individuals to make informed decisions regarding continuation or termination of a pregnancy, and this is particularly relevant when there is significant fetal damage due to Zika infection [246,247].

Conclusions

As of mid-2019, the Zika virus showed autochthonous mosquito-borne transmission in 87 countries and territories, and opened a new chapter in the book of viral teratogenesis. One of the unique aspects of the Zika virus is that an emerging mosquito-borne infectious disease, which can have teratogenic effects, became intimately intertwined with the access to, and conversations about reproductive health and family planning. The epidemic brought into the public attention several long-known public health crises, including barriers in access to contraception and abortion; inequalities in reproductive health education and messaging; and gender-based violence, all of them playing decisive roles in women’s ability to make reproductive decisions. In context of the teratogenic effects of the Zika virus, an emerging challenge is that in several countries that were affected, abortions are already banned at the time when microcephaly can be detected on ultrasound. In the US, the June 2022 reversal of Roe v. Wade, and the passage of abortion bans and restrictions in several states, along with predictions that broader geographical areas may be impacted in the future as the result of climate change, open important questions on the options that will be available for women with affected pregnancies. The Zika virus epidemic remains an ongoing concern and provides a unique and important case study that brings family planning and reproductive empowerment to the forefront of medicine and public health.

Author Contributions

RAS, AG, and FAC were involved in study conception, planning the design of the paper, and analyzing the data from the literature. RAS, AG, and AK performed the literature search. RAS, AG, and FAC wrote the manuscript, and all authors read, critically reviewed, and edited the final version of the manuscript.

Funding

None to declare.

Conflicts of Interest

All authors – none to declare.

References

  1. Anderson, K.B.; Thomas, S.J.; Endy, T.P. The emergence of Zika Virus: A narrative review. Ann Intern Med 2016, 165, 175–183. [Google Scholar] [CrossRef]
  2. Barbi, L.; Coelho, A.V.C.; Alencar, L.C.A.; Crovella, S. Prevalence of Guillain-Barré syndrome among Zika virus infected cases: A systematic review and meta-analysis. Braz J Infect Dis 2018, 22, 137–141. [Google Scholar] [CrossRef]
  3. Musso, D.; Gubler, D.J. Zika Virus. Clin Microbiol Rev 2016, 29, 487–524. [Google Scholar] [CrossRef]
  4. Zanluca, C.; Melo, V.C.; Mosimann, A.L.; Santos, G.I.; Santos, C.N.; Luz, K. First report of autochthonous transmission of Zika virus in Brazil. Mem Inst Oswaldo Cruz 2015, 110, 569–572. [Google Scholar] [CrossRef]
  5. Imperato, P.J. The convergence of a virus, mosquitoes, and human travel in globalizing the Zika epidemic. J Community Health 2016, 41, 674–679. [Google Scholar] [CrossRef]
  6. Plourde, A.R.; Bloch, E.M. A literature review of Zika virus. Emerg Infect Dis 2016, 22, 1185–1192. [Google Scholar] [CrossRef]
  7. Fellner, C. Zika virus: Anatomy of a global health crisis. P T 2016, 41, 242–253. [Google Scholar]
  8. Kindhauser, M.K.; Allen, T.; Frank, V.; Santhana, R.S.; Dye, C. Zika: The origin and spread of a mosquito-borne virus. Bull World Health Organ 2016, 94, 675–686c. [Google Scholar] [CrossRef]
  9. Dick, G.W.; Kitchen, S.F.; Haddow, A.J. Zika virus. I. Isolations and serological specificity. Trans R Soc Trop Med Hyg 1952, 46, 509–520. [Google Scholar] [CrossRef]
  10. Simpson, D.I. Zika virus infection in man. Trans R Soc Trop Med Hyg 1964, 58, 335–338. [Google Scholar] [CrossRef] [PubMed]
  11. Duffy, M.R.; Chen, T.H.; Hancock, W.T.; et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 2009, 360, 2536–2543. [Google Scholar] [CrossRef] [PubMed]
  12. Wikan, N.; Smith, D.R. Zika virus: History of a newly emerging arbovirus. Lancet Infect Dis 2016, 16, e119–e126. [Google Scholar] [CrossRef]
  13. Tognarelli, J.; Ulloa, S.; Villagra, E.; et al. A report on the outbreak of Zika virus on Easter Island, South Pacific, 2014. Arch Virol 2016, 161, 665–668. [Google Scholar] [CrossRef] [PubMed]
  14. Passi, D.; Sharma, S.; Dutta, S.R.; Ahmed, M. Zika virus diseases – the new face of an ancient enemy as global public health emergency (2016): Brief review and recent updates. Int J Prev Med 2017, 8, 6. [Google Scholar] [CrossRef]
  15. Delatorre, E.; Fernández, J.; Bello, G. Investigating the role of Easter Island in migration of Zika virus from South Pacific to Americas. Emerg Infect Dis 2018, 24, 2119–2121. [Google Scholar] [CrossRef]
  16. de Araújo, T.V.B.; Ximenes, R.A.A.; Miranda-Filho, D.B.; et al. Association between microcephaly, Zika virus infection, and other risk factors in Brazil: Final report of a case-control study. Lancet Infect Dis 2018, 18, 328–336. [Google Scholar] [CrossRef]
  17. Hennessey, M.; Fischer, M.; Staples, J.E. Zika virus spreads to new areas - Region of the Americas, May 2015-January 2016. MMWR Morb Mortal Wkly Rep 2016, 65, 55–58. [Google Scholar] [CrossRef]
  18. Faria, N.R.; Azevedo, R.; Kraemer, M.U.G.; et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science 2016, 352, 345–349. [Google Scholar] [CrossRef] [PubMed]
  19. Grubaugh, N.D.; Saraf, S.; Gangavarapu, K.; et al. Travel surveillance and genomics uncover a hidden Zika outbreak during the waning epidemic. Cell 2019, 178, 1057–1071.e11. [Google Scholar] [CrossRef]
  20. Thomas, D.L.; Sharp, T.M.; Torres, J.; et al. Local transmission of Zika virus–Puerto Rico, November 23, 2015-January 28, 2016. MMWR Morb Mortal Wkly Rep 2016, 65, 154–158. [Google Scholar] [CrossRef]
  21. Ventura, C.V.; Albini, T.A.; Berrocal, A.M. First locally transmitted Zika virus cases identified in the United States. JAMA Ophthalmol 2016, 134, 1219–1220. [Google Scholar] [CrossRef]
  22. Mutebi, J.P.; Godsey, M.; Rose, D.; et al. Entomological investigation following a Zika outbreak in Brownsville, Texas. J Am Mosq Control Assoc 2021, 37, 286–290. [Google Scholar] [CrossRef]
  23. Grubaugh, N.D.; Ladner, J.T.; Kraemer, M.U.G.; et al. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature 2017, 546, 401–405. [Google Scholar] [CrossRef]
  24. McCloskey, B.; Endericks, T. The rise of Zika infection and microcephaly: What can we learn from a public health emergency? Public Health 2017, 150, 87–92. [Google Scholar] [CrossRef] [PubMed]
  25. Hajra, A.; Bandyopadhyay, D.; Hajra, S.K. Zika virus: A global threat to humanity: A comprehensive review and current developments. N Am J Med Sci 2016, 8, 123–128. [Google Scholar] [CrossRef]
  26. Hills, S.L.; Fischer, M.; Petersen, L.R. Epidemiology of Zika virus infection. J Infect Dis 2017, 216, S868–S874. [Google Scholar] [CrossRef] [PubMed]
  27. Harper, D.R.; Litaker, J.; Logan, J. Zika Virus. In eLS; John Wiley & Sons, Ltd., 2018; pp. 1–12. [Google Scholar]
  28. Musso, D.; Ko, A.I.; Baud, D. Zika virus infection - after the pandemic. N Engl J Med 2019, 381, 1444–1457. [Google Scholar] [CrossRef]
  29. Li, S.L.; Messina, J.P.; Pybus, O.G.; Kraemer, M.U.G.; Gardner, L. A review of models applied to the geographic spread of Zika virus. Trans R Soc Trop Med Hyg 2021, 115, 956–964. [Google Scholar] [CrossRef] [PubMed]
  30. Yakob, L. Zika virus after the public health emergency of international concern period, Brazil. Emerg Infect Dis 2022, 28, 837–840. [Google Scholar] [CrossRef]
  31. Correa-Morales, F.; González-Acosta, C.; Mejía-Zúñiga, D.; et al. Surveillance for Zika in Mexico: Naturally infected mosquitoes in urban and semi-urban areas. Pathog Glob Health 2019, 113, 309–314. [Google Scholar] [CrossRef]
  32. Ushijima, Y.; Abe, H.; Mbadinga, M.J.V.M.; et al. Re-emergence of dengue, chikungunya, and Zika viruses in 2021 after a 10-year gap in Gabon. IJID Reg 2022, 5, 68–71. [Google Scholar] [CrossRef]
  33. Khan, E.; Jindal, H.; Mishra, P.; Suvvari, T.K.; Jonna, S. The 2021 Zika outbreak in Uttar Pradesh state of India: Tackling the emerging public health threat. Trop Doct 2022, 52, 474–478. [Google Scholar] [CrossRef]
  34. Bardhan, M.; Pramanik, D.; Riyaz, R.; Hasan, M.M.; Essar, M.Y. Dual burden of Zika and COVID-19 in India: Challenges, opportunities and recommendations. Trop Med Health 2021, 49, 83. [Google Scholar] [CrossRef] [PubMed]
  35. Yadav, P.D.; Kaur, H.; Gupta, N.; et al. Zika a vector borne disease detected in newer states of India amidst the COVID-19 pandemic. Front Microbiol 2022, 13, 888195. [Google Scholar] [CrossRef]
  36. Grant, R.; Kizu, J.; Graham, M.; et al. Serological evidence of possible high levels of undetected transmission of Zika virus among Papua New Guinea military personnel, 2019. IJID Reg 2022, 4, 131–133. [Google Scholar] [CrossRef]
  37. Angelo, K.M.; Stoney, R.J.; Brun-Cottan, G.; et al. Zika among international travellers presenting to GeoSentinel sites, 2012-2019: Implications for clinical practice. J Travel Med 2020, 27, taaa061. [Google Scholar] [CrossRef]
  38. Sapkal, G.N.; Yadav, P.D.; Vegad, M.M.; Viswanathan, R.; Gupta, N.; Mourya, D.T. First laboratory confirmation on the existence of Zika virus disease in India. J Infect 2018, 76, 314–317. [Google Scholar] [CrossRef]
  39. Yadav, P.D.; Niyas, V.K.M.; Arjun, R.; et al. Detection of Zika virus disease in Thiruvananthapuram, Kerala, India 2021 during the second wave of COVID-19 pandemic. J Med Virol 2022, 94, 2346–2349. [Google Scholar] [CrossRef]
  40. Rawal, G.; Yadav, S.; Kumar, R. Zika virus: An overview. J Family Med Prim Care 2016, 5, 523–527. [Google Scholar] [CrossRef]
  41. Hastings, A.K.; Fikrig, E. Zika virus and sexual transmission: A new route of transmission for mosquito-borne flaviviruses. Yale J Biol Med 2017, 90, 325–330. [Google Scholar] [PubMed]
  42. Besnard, M.; Lastere, S.; Teissier, A.; Cao-Lormeau, V.; Musso, D. Evidence of perinatal transmission of Zika virus, French Polynesia, December 2013 and February 2014. Euro Surveill 2014, 19, 20751. [Google Scholar] [CrossRef] [PubMed]
  43. Lessler, J.; Chaisson, L.H.; Kucirka, L.M.; et al. Assessing the global threat from Zika virus. Science 2016, 353, aaf8160. [Google Scholar] [CrossRef] [PubMed]
  44. Magnus, M.M.; Espósito, D.L.A.; Costa, V.A.D.; et al. Risk of Zika virus transmission by blood donations in Brazil. Hematol Transfus Cell Ther 2018, 40, 250–254. [Google Scholar] [CrossRef]
  45. Gregory, C.J.; Oduyebo, T.; Brault, A.C.; et al. Modes of transmission of Zika Virus. J Infect Dis 2017, 216, S875–S883. [Google Scholar] [CrossRef] [PubMed]
  46. Nogueira, M.L.; Estofolete, C.F.; Terzian, A.C.; et al. Zika virus infection and solid organ transplantation: A new challenge. Am J Transplant 2017, 17, 791–795. [Google Scholar] [CrossRef]
  47. Lowe, R.; Barcellos, C.; Brasil, P.; et al. The Zika virus epidemic in Brazil: From discovery to future implications. Int J Environ Res Public Health 2018, 15, 96. [Google Scholar] [CrossRef]
  48. Centeno-Tablante, E.; Medina-Rivera, M.; Finkelstein, J.L.; et al. Update on the transmission of Zika virus through breast milk and breastfeeding: A systematic review of the evidence. Viruses 2021, 13, 123. [Google Scholar] [CrossRef]
  49. Sampieri, C.L.; Montero, H. Breastfeeding in the time of Zika: A systematic literature review. PeerJ 2019, 7, e6452. [Google Scholar] [CrossRef]
  50. Song, B.H.; Yun, S.I.; Woolley, M.; Lee, Y.M. Zika virus: History, epidemiology, transmission, and clinical presentation. J Neuroimmunol 2017, 308, 50–64. [Google Scholar] [CrossRef]
  51. Harris, L.H.; Silverman, N.S.; Marshall, M.F. The paradigm of the paradox: Women, pregnant women, and the unequal burdens of the Zika virus pandemic. Am J Bioeth 2016, 16, 1–4. [Google Scholar] [CrossRef]
  52. Manangeeswaran, M.; Kielczewski, J.L.; Sen, H.N.; et al. ZIKA virus infection causes persistent chorioretinal lesions. Emerg Microbes Infect 2018, 7, 96. [Google Scholar] [CrossRef] [PubMed]
  53. Scatularo, C.E.; Ballesteros, O.A.; Saldarriaga, C.; et al. Zika & heart: A systematic review. Trends Cardiovasc Med 2022, 32, 52–58. [Google Scholar]
  54. Carta, K.A.G.; Mendoza, I.; Morr, I.; et al. Myocarditis, heart failure and arrhythmias in patients with Zika. J Am Coll Cardiol 2017, 69, 906. [Google Scholar] [CrossRef]
  55. Li, H.; Saucedo-Cuevas, L.; Shresta, S.; Gleeson, J.G. The neurobiology of Zika virus. Neuron 2016, 92, 949–958. [Google Scholar] [CrossRef]
  56. Mittal, R.; Nguyen, D.; Debs, L.H.; et al. Zika virus: An emerging global health threat. Front Cell Infect Microbiol 2017, 7, 486. [Google Scholar] [CrossRef]
  57. Jaenisch, T.; Rosenberger, K.D.; Brito, C.; Brady, O.; Brasil, P.; Marques, E.T. Risk of microcephaly after Zika virus infection in Brazil, 2015 to 2016. Bull World Health Organ 2017, 95, 191–198. [Google Scholar] [CrossRef]
  58. Ming, G.L.; Song, H.; Tang, H. Racing to uncover the link between Zika virus and microcephaly. Cell Stem Cell 2017, 20, 749–753. [Google Scholar] [CrossRef] [PubMed]
  59. Parens, R.; Nijhout, H.F.; Morales, A.; Xavier Costa, F.; Bar-Yam, Y. A possible link between pyriproxyfen and microcephaly. PLoS Curr 2017, 9, ecurrents.outbreaks.5afb0bfb8cf31d9a4baba7b19b4edbac. [Google Scholar] [CrossRef] [PubMed]
  60. Brasil, P.; Pereira, J.P., Jr.; Moreira, M.E.; et al. Zika virus infection in pregnant women in Rio de Janeiro. N Engl J Med 2016, 375, 2321–2334. [Google Scholar] [CrossRef]
  61. de Araújo, T.V.B.; Rodrigues, L.C.; de Alencar Ximenes, R.A.; et al. Association between Zika virus infection and microcephaly in Brazil, January to May, 2016: Preliminary report of a case-control study. Lancet Infect Dis 2016, 16, 1356–1363. [Google Scholar] [CrossRef]
  62. Rasmussen, S.A.; Jamieson, D.J.; Honein, M.A.; Petersen, L.R. Zika virus and birth defects–reviewing the evidence for causality. N Engl J Med 2016, 374, 1981–1987. [Google Scholar] [CrossRef]
  63. Cauchemez, S.; Besnard, M.; Bompard, P.; et al. Association between Zika virus and microcephaly in French Polynesia, 2013–2015: A retrospective study. Lancet 2016, 387, 2125–2132. [Google Scholar] [CrossRef]
  64. Marinho, F.; Araújo, V.E.; Porto, D.L.; et al. Microcephaly in Brazil: Prevalence and characterization of cases from the Information System on Live Births (Sinasc), 2000-2015. Epidemiol Serv Saude 2016, 25, 701–712. [Google Scholar] [CrossRef] [PubMed]
  65. Driggers, R.W.; Ho, C.Y.; Korhonen, E.M.; et al. Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N Engl J Med 2016, 374, 2142–2151. [Google Scholar] [CrossRef] [PubMed]
  66. Regadas, V.C.; Silva, M.C.E.; Abud, L.G.; et al. Microcephaly caused by congenital Zika virus infection and viral detection in maternal urine during pregnancy. Rev Assoc Med Bras (1992) 2018, 64, 11–14. [Google Scholar] [CrossRef]
  67. Mlakar, J.; Korva, M.; Tul, N.; et al. Zika virus associated with microcephaly. N Engl J Med 2016, 374, 951–958. [Google Scholar] [CrossRef]
  68. Calvet, G.; Aguiar, R.S.; Melo, A.S.O.; et al. Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: A case study. Lancet Infect Dis 2016, 16, 653–660. [Google Scholar] [CrossRef] [PubMed]
  69. Simoni, M.K.; Jurado, K.A.; Abrahams, V.M.; Fikrig, E.; Guller, S. Zika virus infection of Hofbauer cells. Am J Reprod Immunol 2017, 77, 10.1111/aji.12613. [Google Scholar] [CrossRef]
  70. Jurado, K.A.; Simoni, M.K.; Tang, Z.; et al. Zika virus productively infects primary human placenta-specific macrophages. JCI Insight 2016, 1, e88461. [Google Scholar] [CrossRef]
  71. Tang, Z.; Tadesse, S.; Norwitz, E.; Mor, G.; Abrahams, V.M.; Guller, S. Isolation of hofbauer cells from human term placentas with high yield and purity. Am J Reprod Immunol 2011, 66, 336–348. [Google Scholar] [CrossRef]
  72. Bhatnagar, J.; Rabeneck, D.B.; Martines, R.B.; et al. Zika virus RNA replication and persistence in brain and placental tissue. Emerg Infect Dis 2017, 23, 405–414. [Google Scholar] [CrossRef] [PubMed]
  73. Wang, J.N.; Ling, F. Zika virus infection and microcephaly: Evidence for a causal link. Int J Environ Res Public Health 2016, 13, 1031. [Google Scholar] [CrossRef]
  74. Nunes, M.L.; Carlini, C.R.; Marinowic, D.; et al. Microcephaly and Zika virus: A clinical and epidemiological analysis of the current outbreak in Brazil. J Pediatr (Rio J) 2016, 92, 230–240. [Google Scholar] [CrossRef]
  75. Krauer, F.; Riesen, M.; Reveiz, L.; et al. Zika virus infection as a cause of congenital brain abnormalities and Guillain-Barré syndrome: Systematic review. PLoS Med 2017, 14, e1002203. [Google Scholar] [CrossRef]
  76. Honein, M.A.; Dawson, A.L.; Petersen, E.E.; et al. Birth defects among fetuses and infants of US women with evidence of possible Zika virus infection during pregnancy. JAMA 2017, 317, 59–68. [Google Scholar] [CrossRef]
  77. Mehrjardi, M.Z. Is Zika virus an emerging TORCH agent? An invited commentary. Virology (Auckl) 2017, 8, 1178122x17708993. [Google Scholar] [CrossRef]
  78. Brady, O.J.; Osgood-Zimmerman, A.; Kassebaum, N.J.; et al. The association between Zika virus infection and microcephaly in Brazil 2015-2017: An observational analysis of over 4 million births. PLoS Med 2019, 16, e1002755. [Google Scholar] [CrossRef]
  79. Yuan, L.; Huang, X.Y.; Liu, Z.Y.; et al. A single mutation in the prM protein of Zika virus contributes to fetal microcephaly. Science 2017, 358, 933–936. [Google Scholar] [CrossRef] [PubMed]
  80. Costa, F.; Ko, A.I. Zika virus and microcephaly: Where do we go from here? Lancet Infect Dis 2018, 18, 236–237. [Google Scholar] [CrossRef] [PubMed]
  81. Zorrilla, C.D.; García García, I.; García Fragoso, L.; De La Vega, A. Zika virus infection in pregnancy: Maternal, fetal, and neonatal considerations. J Infect Dis 2017, 216, S891–S896. [Google Scholar] [CrossRef]
  82. Melo, A.S.; Aguiar, R.S.; Amorim, M.M.; et al. Congenital Zika virus infection: Beyond neonatal microcephaly. JAMA Neurol 2016, 73, 1407–1416. [Google Scholar] [CrossRef]
  83. Castro, J.D.V.; Pereira, L.P.; Dias, D.A.; et al. Presumed Zika virus-related congenital brain malformations: The spectrum of CT and MRI findings in fetuses and newborns. Arq Neuropsiquiatr 2017, 75, 703–710. [Google Scholar] [CrossRef]
  84. Moore, C.A.; Staples, J.E.; Dobyns, W.B.; et al. Characterizing the pattern of anomalies in congenital Zika syndrome for pediatric clinicians. JAMA Pediatr 2017, 171, 288–295. [Google Scholar] [CrossRef]
  85. van der Linden, V.; Pessoa, A.; Dobyns, W.; et al. Description of 13 infants born during October 2015-January 2016 with congenital Zika virus infection without microcephaly at birth - Brazil. MMWR Morb Mortal Wkly Rep 2016, 65, 1343–1348. [Google Scholar] [CrossRef]
  86. Klase, Z.A.; Khakhina, S.; Schneider Ade, B.; Callahan, M.V.; Glasspool-Malone, J.; Malone, R. Zika fetal neuropathogenesis: Etiology of a viral syndrome. PLoS Negl Trop Dis 2016, 10, e0004877. [Google Scholar] [CrossRef]
  87. Tahotná, A.; Brucknerová, J.; Brucknerová, I. Zika virus infection from a newborn point of view. TORCH or TORZiCH? Interdiscip Toxicol 2018, 11, 241–246. [Google Scholar] [CrossRef] [PubMed]
  88. Garcia Serpa Osorio-de-Castro, C.; Silva Miranda, E.; Machado de Freitas, C.; Rochel de Camargo, K., Jr.; Cranmer, H.H. The Zika virus outbreak in Brazil: Knowledge gaps and challenges for risk reduction. Am J Public Health 2017, 107, 960–965. [Google Scholar] [CrossRef]
  89. Diaz-Quijano, F.A.; Pelissari, D.M.; Chiavegatto Filho, A.D.P. Zika-associated microcephaly epidemic and birth rate reduction in Brazilian cities. Am J Public Health 2018, 108, 514–516. [Google Scholar] [CrossRef]
  90. Roa, M. Zika virus outbreak: Reproductive health and rights in Latin America. Lancet 2016, 387, 843. [Google Scholar] [CrossRef] [PubMed]
  91. Panchaud, A.; Stojanov, M.; Ammerdorffer, A.; Vouga, M.; Baud, D. Emerging role of Zika virus in adverse fetal and neonatal outcomes. Clin Microbiol Rev 2016, 29, 659–694. [Google Scholar] [CrossRef] [PubMed]
  92. Chang, C.; Ortiz, K.; Ansari, A.; Gershwin, M.E. The Zika outbreak of the 21st century. J Autoimmun 2016, 68, 1–13. [Google Scholar] [CrossRef]
  93. Samarasekera, U.; Triunfol, M. Concern over Zika virus grips the world. Lancet 2016, 387, 521–524. [Google Scholar] [CrossRef]
  94. Alter, C. Why Latin American women can’t follow the Zika advice to avoid pregnancy. Time. 29 January 2016. Available online: http://time.com/4197318/zika-virus-latin-america-avoid-pregnancy/ (accessed on 5 February 2022).
  95. Hodge, J.G.; Corbett, A.; Repka, A.; Judd, P.J. Zika virus and global implications for reproductive health reforms. Disaster Med Public Health Prep 2016, 10, 713–715. [Google Scholar] [CrossRef] [PubMed][Green Version]
  96. Vélez, A.C.; Diniz, S.G. Inequality, Zika epidemics, and the lack of reproductive rights in Latin America. Reprod Health Matters 2016, 24, 57–61. [Google Scholar] [CrossRef]
  97. Byron, K.; Howard, D. ‘Hey everybody, don’t get pregnant’: Zika, WHO and an ethical framework for advising. J Med Ethics 2017, 43, 334–338. [Google Scholar] [CrossRef] [PubMed]
  98. Aiken, A.; Aiken, C.E.; Trussell, J. In the midst of Zika pregnancy advisories, termination of pregnancy is the elephant in the room. BJOG 2017, 124, 546–548. [Google Scholar] [CrossRef] [PubMed]
  99. World Health Organization. Prevention of sexual transmission of Zika virus: Interim guidance update. 2016. Available online: http://apps.who.int/iris/bitstream/10665/204421/1/WHO_ZIKV_MOC_16.1_eng.pdf (accessed on 2 July 2022).
  100. McNeil, D.G., Jr. Delay pregnancy in areas with Zika, W.H.O. suggests. The New York Times. 9 June 2016. Available online: https://www.nytimes.com/2016/06/10/health/zika-virus-pregnancy-who.html (accessed on 2 July 2022).
  101. Burke, A.; Moreau, C. Family planning and Zika virus: The power of prevention. Semin Reprod Med 2016, 34, 305–312. [Google Scholar] [CrossRef] [PubMed]
  102. Ali, M.; Miller, K.; Folz, R.; Johnson, B.R., Jr.; Kiarie, J. Study protocol on establishment of sentinel sites network for contraceptive and abortion trends, needs and utilization of services in Zika virus affected countries. Reprod Health 2017, 14, 19. [Google Scholar] [CrossRef] [PubMed]
  103. Darney, B.G.; Aiken, A.R.A.; Küng, S. Access to contraception in the context of Zika: Health system challenges and responses. Obstet Gynecol 2017, 129, 638–642. [Google Scholar] [CrossRef] [PubMed]
  104. Coyne, C.B.; Lazear, H.M. Zika virus - reigniting the TORCH. Nat Rev Microbiol 2016, 14, 707–715. [Google Scholar] [CrossRef] [PubMed]
  105. Collucci, C. Brazilian attorneys demand abortion rights for women infected with Zika. BMJ 2016, 354, i4657. [Google Scholar] [CrossRef][Green Version]
  106. Gressick, K.; Gelpi, A.; Chanroo, T. Zika and abortion in Brazilian newspapers: How a new outbreak revived an old debate on reproductive rights. Sex Reprod Health Matters 2019, 27, 1586818. [Google Scholar] [CrossRef]
  107. Wenham, C.; Arevalo, A.; Coast, E.; et al. Zika, abortion and health emergencies: A review of contemporary debates. Global Health 2019, 15, 49. [Google Scholar] [CrossRef]
  108. Schuck-Paim, C.; Lopez, D.; Simonsen, L.; Alonso, W. Unintended pregnancies in Brazil - a challenge for the recommendation to delay pregnancy due to Zika. PLoS Curr 2016, 8, ecurrents.outbreaks.7038a6813f734c1db547240c2a0ba291. [Google Scholar] [CrossRef] [PubMed]
  109. Sedgh, G.; Singh, S.; Hussain, R. Intended and unintended pregnancies worldwide in 2012 and recent trends. Stud Fam Plann 2014, 45, 301–314. [Google Scholar] [CrossRef] [PubMed]
  110. Theme-Filha, M.M.; Baldisserotto, M.L.; Fraga, A.C.; Ayers, S.; da Gama, S.G.; Leal, M.D. Factors associated with unintended pregnancy in Brazil: Cross-sectional results from the Birth in Brazil National Survey, 2011/2012. Reprod Health 2016, 13, 118. [Google Scholar] [CrossRef]
  111. Le, H.H.; Connolly, M.P.; Bahamondes, L.; Cecatti, J.G.; Yu, J.; Hu, H.X. The burden of unintended pregnancies in Brazil: A social and public health system cost analysis. Int J Womens Health 2014, 6, 663–670. [Google Scholar] [CrossRef]
  112. Melo, C.R.M.E.; Borges, A.L.V.; Duarte, L.S.; Nascimento, N.C. Contraceptive use and the intention to become pregnant among women attending the Brazilian Unified Health System. Rev Lat Am Enfermagem 2020, 28, e3328. [Google Scholar] [CrossRef]
  113. Goicolea, I.; San Sebastian, M. Unintended pregnancy in the amazon basin of Ecuador: A multilevel analysis. Int J Equity Health 2010, 9, 14. [Google Scholar] [CrossRef]
  114. Córdova Pozo, K.; Chandra-Mouli, V.; Decat, P.; et al. Improving adolescent sexual and reproductive health in Latin America: Reflections from an International Congress. Reprod Health 2015, 12, 11. [Google Scholar] [CrossRef] [PubMed]
  115. Rodríguez Ribas, C. Adolescent pregnancy, public policies, and targeted programs in Latin America and the Caribbean: A systematic review. Rev Panam Salud Publica 2021, 45, e144. [Google Scholar] [CrossRef] [PubMed]
  116. Decat, P.; Nelson, E.; De Meyer, S.; et al. Community embedded reproductive health interventions for adolescents in Latin America: Development and evaluation of a complex multi-centre intervention. BMC Public Health 2013, 13, 31. [Google Scholar] [CrossRef] [PubMed]
  117. Ivanova, O.; Cordova-Pozo, K.; Segura, Z.E.; et al. Lessons learnt from the CERCA Project, a multicomponent intervention to promote adolescent sexual and reproductive health in three Latin America countries: A qualitative post-hoc evaluation. Eval Program Plann 2016, 58, 98–105. [Google Scholar] [CrossRef]
  118. Dansereau, E.; Schaefer, A.; Hernández, B.; et al. Perceptions of and barriers to family planning services in the poorest regions of Chiapas, Mexico: A qualitative study of men, women, and adolescents. Reprod Health 2017, 14, 129. [Google Scholar] [CrossRef]
  119. Lopez, C.; Ramirez, D.C.; Valenzuela, J.I.; et al. Sexual and reproductive health for young adults in Colombia: Teleconsultation using mobile devices. JMIR Mhealth Uhealth 2014, 2, e38. [Google Scholar] [CrossRef]
  120. Garraza, L.G.; Tobar, F.; Rodríguez Bernate, I. Out-of-pocket spending for contraceptives in Latin America. Sex Reprod Health Matters 2020, 28, 1833429. [Google Scholar] [CrossRef]
  121. Fagan, T.; Dutta, A.; Rosen, J.; Olivetti, A.; Klein, K. Family planning in the context of Latin America’s universal health coverage agenda. Glob Health Sci Pract 2017, 5, 382–398. [Google Scholar] [CrossRef]
  122. Ponce de Leon, R.G.; Ewerling, F.; Serruya, S.J.; et al. Contraceptive use in Latin America and the Caribbean with a focus on long-acting reversible contraceptives: Prevalence and inequalities in 23 countries. Lancet Glob Health 2019, 7, e227–e235. [Google Scholar] [CrossRef]
  123. Bahamondes, L.; Villarroel, C.; Frías Guzmán, N.; Oizerovich, S.; Velázquez-Ramírez, N.; Monteiro, I. The use of long-acting reversible contraceptives in Latin America and the Caribbean: Current landscape and recommendations. Hum Reprod Open 2018, 2018, hox030. [Google Scholar] [CrossRef] [PubMed]
  124. Gakidou, E.; Vayena, E. Use of modern contraception by the poor is falling behind. PLoS Med 2007, 4, e31. [Google Scholar] [CrossRef][Green Version]
  125. Dehlendorf, C.; Rodriguez, M.I.; Levy, K.; Borrero, S.; Steinauer, J. Disparities in family planning. Am J Obstet Gynecol 2010, 202, 214–220. [Google Scholar] [CrossRef]
  126. Fernandes Moron, A. Zika virus outbreak and reproductive rights. BJOG 2017, 124, 549. [Google Scholar] [CrossRef][Green Version]
  127. Rasanathan, J.J.; MacCarthy, S.; Diniz, D.; Torreele, E.; Gruskin, S. Engaging human rights in the response to the evolving Zika virus epidemic. Am J Public Health 2017, 107, 525–531. [Google Scholar] [CrossRef]
  128. Feld, H.; Rojas, V.; Linares, A.M. “We keep quiet”: Exploring the context of pregnancy intention in a low-resource community in Ecuador. Sex Reprod Health Matters 2019, 27, 1686198. [Google Scholar] [CrossRef] [PubMed]
  129. Gakidou, E.; Vayena, E. Use of modern contraception by the poor is falling behind. PLOS Med 2007, 4, e31. [Google Scholar] [CrossRef][Green Version]
  130. Haider, S.; Stoffel, C.; Donenberg, G.; Geller, S. Reproductive health disparities: A focus on family planning and prevention among minority women and adolescents. Glob Adv Health Med 2013, 2, 94–99. [Google Scholar] [CrossRef]
  131. Grady, C.D.; Dehlendorf, C.; Cohen, E.D.; Schwarz, E.B.; Borrero, S. Racial and ethnic differences in contraceptive use among women who desire no future children, 2006-2010 National Survey of Family Growth. Contraception 2015, 92, 62–70. [Google Scholar] [CrossRef]
  132. Dansereau, E.; McNellan, C.R.; Gagnier, M.C.; et al. Coverage and timing of antenatal care among poor women in 6 Mesoamerican countries. BMC Pregnancy Childbirth 2016, 16, 234. [Google Scholar] [CrossRef]
  133. Bearak, J.; Popinchalk, A.; Alkema, L.; Sedgh, G. Global, regional, and subregional trends in unintended pregnancy and its outcomes from 1990 to 2014: Estimates from a Bayesian hierarchical model. Lancet Glob Health 2018, 6, e380–e389. [Google Scholar] [CrossRef] [PubMed]
  134. Shakya, H.B.; Darmstadt, G.L.; Barker, K.M.; Weeks, J.; Christakis, N.A. Social normative and social network factors associated with adolescent pregnancy: A cross-sectional study of 176 villages in rural Honduras. J Glob Health 2020, 10, 010706. [Google Scholar] [CrossRef] [PubMed]
  135. Gillespie, D.; Ahmed, S.; Tsui, A.; Radloff, S. Unwanted fertility among the poor: An inequity? Bull World Health Organ 2007, 85, 100–107. [Google Scholar] [CrossRef]
  136. O’Kelly, B.; Lambert, J.S. Vector-borne diseases in pregnancy. Ther Adv Infect Dis 2020, 7, 2049936120941725. [Google Scholar] [CrossRef]
  137. Langer, A.; Caglia, J.M.; Menendez, C. Sexual and reproductive health and rights in the time of Zika in Latin America and the Caribbean. Stud Fam Plann 2016, 47, 179–181. [Google Scholar] [CrossRef]
  138. Gurman, T.; Ballard Sara, A.; Villanueva Lorenzo, F.; et al. The role of gender in Zika prevention behaviors in the Dominican Republic: Findings and programmatic implications from a qualitative study. PLoS Negl Trop Dis 2020, 14, e0007994. [Google Scholar] [CrossRef]
  139. Marbán-Castro, E.; Villén-Gonzalvo, A.; Enguita-Fernàndez, C.; et al. Uncertainties, fear and stigma: Perceptions of Zika virus among pregnant women in Spain. Int J Environ Res Public Health 2020, 17, 6643. [Google Scholar] [CrossRef]
  140. Wenham, C.; Abagaro, C.; Arévalo, A.; et al. Analysing the intersection between health emergencies and abortion during Zika in Brazil, El Salvador and Colombia. Soc Sci Med 2021, 270, 113671. [Google Scholar] [CrossRef]
  141. Gerdts, C.; DePiñeres, T.; Hajri, S.; et al. Denial of abortion in legal settings. J Fam Plann Reprod Health Care 2015, 41, 161–163. [Google Scholar] [CrossRef] [PubMed]
  142. Finer, L.; Fine, J.B. Abortion law around the world: Progress and pushback. Am J Public Health 2013, 103, 585–589. [Google Scholar] [CrossRef]
  143. Rodgers, Y.V.M.; Coast, E.; Lattof, S.R.; Poss, C.; Moore, B. The macroeconomics of abortion: A scoping review and analysis of the costs and outcomes. PLoS ONE 2021, 16, e0250692. [Google Scholar] [CrossRef] [PubMed]
  144. Viterna, J.; Bautista, J.S.G. Pregnancy and the 40-year prison sentence: How “Abortion is murder” became institutionalized in the Salvadoran judicial system. Health Hum Rights 2017, 19, 81–93. [Google Scholar] [PubMed]
  145. Cortez, R.; Revuelta, K.A.; Guirola, Y. Adolescent sexual and reproductive health in El Salvador, Health, Nutrition and Population (HNP); Discussion Paper; Family of the World Bank Human Development Network: Washington DC, USA, 2015. [Google Scholar]
  146. Luna, F. Public health agencies’ obligations and the case of Zika. Bioethics 2017, 31, 575–581. [Google Scholar] [CrossRef]
  147. Torjesen, I. Rape survivor is sentenced to 30 years in jail under El Salvador’s extreme anti-abortion law. BMJ 2017, 358, j3327. [Google Scholar] [CrossRef]
  148. The American Bar Association. Trial observation report: Criminal trial of Evelyn Hernandez in El Salvador. 2020. Available online: https://www.americanbar.org/groups/human_rights/reports/trial-observation-report–criminal-trial-of-evelyn-hernandez-in-/ (accessed on 19 May 2022).
  149. Kennedy, M. Salvadoran woman who lost her pregnancy is acquitted of homicide in retrial. 2019. Available online: https://www.npr.org/2019/08/20/752731596/el-salvador-woman-who-lost-her-pregnancy-is-acquitted-of-homicide-in-retrial.
  150. Arie, S. Seriously ill woman expecting a baby with anencephaly has waited a month to learn whether she can have an abortion. BMJ 2013, 346, f2814. [Google Scholar] [CrossRef] [PubMed]
  151. Morgan, L.M. The Dublin Declaration on maternal health care and anti-abortion activism: Examples from Latin America. Health Hum Rights 2017, 19, 41–53. [Google Scholar] [PubMed]
  152. Redacción Nacional. “Todas las embarazadas con zika tienen la opción de abortar”: Women’s Link Worldwide. 21 January 2016. Available online: https://www.elespectador.com/noticias/nacional/todas-embarazadas-zika-tienen-opcion-de-abortar-womens-articulo-612046 (accessed on 10 March 2018).
  153. Carabali, M.; Austin, N.; King, N.B.; Kaufman, J.S. The Zika epidemic and abortion in Latin America: A scoping review. Glob Health Res Policy 2018, 3, 15. [Google Scholar] [CrossRef] [PubMed]
  154. Sun, L.H. WHO: People in Zika-affected regions should consider delaying pregnancy. The Washington Post. 9 June 2016. Available online: https://www.washingtonpost.com/news/to-your-health/wp/2016/06/09/who-women-in-zika-affected-regions-should-consider-delaying-pregnancy/ (accessed on 30 June 2022).
  155. Coutinho, R.Z.; Montalvo, A.V.; Weitzman, A.; Marteleto, L.J. Zika virus public health crisis and the perpetuation of gender inequality in Brazil. Reprod Health 2021, 18, 40. [Google Scholar] [CrossRef]
  156. Osamor, P.E.; Grady, C. Zika virus: Promoting male involvement in the health of women and families. PLoS Negl Trop Dis 2016, 10, e0005127. [Google Scholar] [CrossRef]
  157. Yamey, G. Sexual and reproductive health: What about boys and men? Education and service provision are the keys to increasing involvement. BMJ 1999, 319, 1315–1316. [Google Scholar] [CrossRef]
  158. Nguyen, B.T.; Schickler, R. Of mosquitoes and men: Mitigating Zika risk via men’s family planning and male contraception. Contracept Reprod Med 2018, 3, 17. [Google Scholar] [CrossRef]
  159. Ribeiro, B.; Hartley, S.; Nerlich, B.; Jaspal, R. Media coverage of the Zika crisis in Brazil: The construction of a ‘war’ frame that masked social and gender inequalities. Soc Sci Med 2018, 200, 137–144. [Google Scholar] [CrossRef]
  160. Kågesten, A.; Bajos, N.; Bohet, A.; Moreau, C. Male experiences of unintended pregnancy: Characteristics and prevalence. Hum Reprod 2015, 30, 186–196. [Google Scholar] [CrossRef]
  161. Casas, X. They are girls, not mothers: The violence of forcing motherhood on young girls in Latin America. Health Hum Rights 2019, 21, 157–167. [Google Scholar]
  162. Bott, S.; Guedes, A.; Ruiz-Celis, A.P.; Mendoza, J.A. Intimate partner violence in the Americas: A systematic review and reanalysis of national prevalence estimates. Rev Panam Salud Publica 2019, 43, e26. [Google Scholar] [CrossRef]
  163. De Meyer, S.; Jaruseviciene, L.; Zaborskis, A.; et al. A cross-sectional study on attitudes toward gender equality, sexual behavior, positive sexual experiences, and communication about sex among sexually active and non-sexually active adolescents in Bolivia and Ecuador. Glob Health Action 2014, 7, 24089. [Google Scholar] [CrossRef]
  164. Torres, V.M.; Goicolea, I.; Edin, K.; Ohman, A. ‘Expanding your mind’: The process of constructing gender-equitable masculinities in young Nicaraguan men participating in reproductive health or gender training programs. Glob Health Action 2012, 5. [Google Scholar] [CrossRef]
  165. Haack, S.L.; Mazar, I.; Carter, E.M.; et al. Cultural sensitivity and global pharmacy engagement in Latin America: Argentina, Brazil, Ecuador, Guatemala, and Mexico. Am J Pharm Educ 2019, 83, 7218. [Google Scholar] [CrossRef]
  166. UN News. Upholding women’s human rights essential to Zika response – UN rights chief. 5 February 2016. Available online: https://news.un.org/en/story/2016/02/521662-upholding-womens-human-rights-essential-zika-response-un-rights-chief (accessed on 6 February 2022).
  167. Wenham, C.; Nunes, J.; Correa Matta, G.; de Oliveira Nogueira, C.; Aparecida Valente, P.; Pimenta, D.N. Gender mainstreaming as a pathway for sustainable arbovirus control in Latin America. PLoS Negl Trop Dis 2020, 14, e0007954. [Google Scholar] [CrossRef] [PubMed]
  168. Stolow, J.; Kendall, C.; Marto Leal Pinheiro, F.; et al. Fertility decision-making during the Zika virus epidemic in Brazil: Where is the decision? Sex Reprod Healthc 2022, 32, 100722. [Google Scholar] [CrossRef] [PubMed]
  169. Rangel, M.A.; Nobles, J.; Hamoudi, A. Brazil’s missing infants: Zika risk changes reproductive behavior. Demography 2020, 57, 1647–1680. [Google Scholar] [CrossRef]
  170. Marteleto, L.J.; Weitzman, A.; Coutinho, R.Z.; Alves, S.V. Women’s reproductive intentions and behaviors during the Zika epidemic in Brazil. Popul Dev Rev 2017, 43, 199–227. [Google Scholar] [CrossRef] [PubMed]
  171. Gomperts, R.J.; Jelinska, K.; Davies, S.; Gemzell-Danielsson, K.; Kleiverda, G. Using telemedicine for termination of pregnancy with mifepristone and misoprostol in settings where there is no access to safe services. BJOG 2008, 115, 1171–1175; discussion 1175–1178. [Google Scholar] [CrossRef]
  172. Aiken, A.R.; Scott, J.G.; Gomperts, R.; Trussell, J.; Worrell, M.; Aiken, C.E. Requests for abortion in Latin America related to concern about Zika virus exposure. N Engl J Med 2016, 375, 396–398. [Google Scholar] [CrossRef]
  173. Mayor, S. Abortion requests increase in Latin America after Zika warning, figures show. BMJ 2016, 353, i3492. [Google Scholar] [CrossRef] [PubMed][Green Version]
  174. Larrea, S.; Palència, L.; Perez, G. Medical abortion provided by telemedicine to women in Latin America: Complications and their treatment. Gac Sanit 2015, 29, 198–204. [Google Scholar] [CrossRef] [PubMed][Green Version]
  175. Diniz, D. Selective abortion in Brazil: The anencephaly case. Dev World Bioeth 2007, 7, 64–67. [Google Scholar] [CrossRef]
  176. Mudjalieb, A.A. Report of an experience to expand access to legal abortion for rape victims in the city of Rio de Janeiro, Brazil. Cad Saude Publica 2020, 36 (Suppl. 1), e00181219. [Google Scholar] [CrossRef]
  177. De Assis Machado, M.R.; Maciel, D.A. The battle over abortion rights in Brazil’s State Arenas, 1995-2006. Health Hum Rights 2017, 19, 119–132. [Google Scholar] [PubMed]
  178. Faúndes, A.; Leocádio, E.; Andalaft, J. Making legal abortion accessible in Brazil. Reprod Health Matters 2002, 10, 120–127. [Google Scholar] [CrossRef][Green Version]
  179. Ekmekci, E.; Gencdal, S. What’s happening when the pregnancies are not terminated in case of anencephalic fetuses? J Clin Med Res 2019, 11, 332–336. [Google Scholar] [CrossRef][Green Version]
  180. Johnson, S.P.; Sebire, N.J.; Snijders, R.J.; Tunkel, S.; Nicolaides, K.H. Ultrasound screening for anencephaly at 10-14 weeks of gestation. Ultrasound Obstet Gynecol 1997, 9, 14–16. [Google Scholar] [CrossRef]
  181. Imbruglia, L.; Cacciatore, A.; Carrara, S.; et al. Abnormal skull findings in neural tube defects. J Prenat Med 2009, 3, 44–47. [Google Scholar] [PubMed]
  182. Chibueze, E.C.; Parsons, A.J.Q.; Lopes, K.D.S.; et al. Diagnostic accuracy of ultrasound scanning for prenatal microcephaly in the context of Zika virus infection: A systematic review and meta-analysis. Sci Rep 2017, 7, 2310. [Google Scholar] [CrossRef]
  183. Lenharo, M. After Roe v. Wade: US researchers warn of what’s to come. Nature 2022, 607, 15–16. [Google Scholar] [CrossRef]
  184. Kimport, K. Abortion after Dobbs: Defendants, denials, and delays. Sci Adv 2022, 8, eade5327. [Google Scholar] [CrossRef]
  185. Murphy, S. Oklahoma governor signs nation’s strictest abortion law, banning procedure from ‘conception’. 2022. Available online: https://www.pbs.org/newshour/health/oklahoma-governor-signs-nations-strictest-abortion-law-banning-procedure-from-conception (accessed on 30 June 2022).
  186. Davis, M.F. The state of abortion rights in the US. Int J Gynaecol Obstet 2022, 159, 324–329. [Google Scholar] [CrossRef]
  187. Messerly, M. Abortion laws by state: Legal status of abortion changing day-by-day after Roe v. Wade overturned. Politico. 2022. Available online: https://www.politico.com/news/2022/07/06/abortion-laws-states-roe-overturned-00044127 (accessed on 12 October 2022).
  188. Rice, W.S.; Labgold, K.; Peterson, Q.T.; Higdon, M.; Njoku, O. Sociodemographic and service use characteristics of abortion fund cases from six states in the U.S. southeast. Int J Environ Res Public Health 2021, 18, 3813. [Google Scholar] [CrossRef]
  189. Tanne, J.H. Texas’s new abortion law is an attack on medical practice and women’s rights, say doctors. BMJ 2021, 374, n2176. [Google Scholar] [CrossRef]
  190. Gallo, M.F.; Casterline, J.B.; Chakraborty, P.; Norris, A.; Bessett, D.; Turner, A.N. Passage of abortion ban and women’s accurate understanding of abortion legality. Am J Obstet Gynecol 2021, 225, e1–e8. [Google Scholar] [CrossRef]
  191. Evans, D.P.; Narasimhan, S. A narrative analysis of anti-abortion testimony and legislative debate related to Georgia’s fetal “heartbeat” abortion ban. Sex Reprod Health Matters 2020, 28, 1686201. [Google Scholar] [CrossRef] [PubMed]
  192. Hahn, M.B.; Eisen, L.; McAllister, J.; Savage, H.M.; Mutebi, J.P.; Eisen, R.J. Updated reported distribution of Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in the United States, 1995-2016. J Med Entomol 2017, 54, 1420–1424. [Google Scholar] [CrossRef]
  193. Powell, J.R.; Tabachnick, W.J. History of domestication and spread of Aedes aegypti–a review. Mem Inst Oswaldo Cruz 2013, 108 (Suppl. 1), 11–17. [Google Scholar] [CrossRef]
  194. Eisen, L.; Moore, C.G. Aedes (Stegomyia) aegypti in the Continental United States: A vector at the cool margin of its geographic range. J Med Entomol 2013, 50, 467–478. [Google Scholar] [CrossRef] [PubMed]
  195. Shacham, E.; Nelson, E.J.; Hoft, D.F.; Schootman, M.; Garza, A. Potential high-risk areas for Zika virus transmission in the contiguous United States. Am J Public Health 2017, 107, 724–731. [Google Scholar] [CrossRef]
  196. Arora, H.S. A to Z of Zika virus: A comprehensive review for clinicians. Glob Pediatr Health 2020, 7, 2333794x20919595. [Google Scholar] [CrossRef]
  197. Sprenger, D.; Wuithiranyagool, T. The discovery and distribution of Aedes albopictus in Harris County, Texas. J Am Mosq Control Assoc 1986, 2, 217–219. [Google Scholar]
  198. Hawley, W.A.; Reiter, P.; Copeland, R.S.; Pumpuni, C.B.; Craig, G.B., Jr. Aedes albopictus in North America: Probable introduction in used tires from northern Asia. Science 1987, 236, 1114–1116. [Google Scholar] [CrossRef] [PubMed]
  199. Khan, S.U.; Ogden, N.H.; Fazil, A.A.; et al. Current and projected distributions of Aedes aegypti and Ae. albopictus in Canada and the U.S. Environmental Health Perspect 2020, 128, 57007. [Google Scholar] [CrossRef] [PubMed]
  200. Kraemer, M.U.; Sinka, M.E.; Duda, K.A.; et al. The global compendium of Aedes aegypti and Ae. albopictus occurrence. Sci Data 2015, 2, 150035. [Google Scholar] [CrossRef]
  201. Little, E.A.H.; Harriott, O.T.; Akaratovic, K.I.; et al. Host interactions of Aedes albopictus, an invasive vector of arboviruses, in Virginia, USA. PLoS Negl Trop Dis 2021, 15, e0009173. [Google Scholar] [CrossRef]
  202. Sun, K.; Zhang, Q.; Pastore-Piontti, A.; et al. Quantifying the risk of local Zika virus transmission in the contiguous US during the 2015-2016 ZIKV epidemic. BMC Med 2018, 16, 195. [Google Scholar] [CrossRef]
  203. Castro, L.A.; Fox, S.J.; Chen, X.; et al. Assessing real-time Zika risk in the United States. BMC Infect Dis 2017, 17, 284. [Google Scholar] [CrossRef]
  204. Sadeghieh, T.; Sargeant, J.M.; Greer, A.L.; et al. Zika virus outbreak in Brazil under current and future climate. Epidemics 2021, 37, 100491. [Google Scholar] [CrossRef]
  205. Ngonghala, C.N.; Ryan, S.J.; Tesla, B.; et al. Effects of changes in temperature on Zika dynamics and control. J R Soc Interface 2021, 18, 20210165. [Google Scholar] [CrossRef]
  206. Ryan, S.J.; Carlson, C.J.; Tesla, B.; et al. Warming temperatures could expose more than 1.3 billion new people to Zika virus risk by 2050. Glob Chang Biol 2021, 27, 84–93. [Google Scholar] [CrossRef]
  207. Chakhtoura, N.; Hazra, R.; Spong, C.Y. Zika virus: A public health perspective. Curr Opin Obstet Gynecol 2018, 30, 116–122. [Google Scholar] [CrossRef] [PubMed]
  208. Freij, B.J.; South, M.A.; Sever, J.L. Maternal rubella and the congenital rubella syndrome. Clin Perinatol 1988, 15, 247–257. [Google Scholar] [CrossRef] [PubMed]
  209. Dunn, P.M. Perinatal lessons from the past: Sir Norman Gregg, ChM, MC, of Sydney (1892-1966) and rubella embryopathy. Arch Dis Child Fetal Neonatal Ed 2007, 92, F513–F514. [Google Scholar] [CrossRef]
  210. Gregg, N.M. Congenital cataract following German measles in the mother. Trans Ophthal Soc Aust 1941, 3, 35–46. [Google Scholar]
  211. Gregg, N.M. Further observations on congenital defects in infants following maternal rubella. Trans Ophthal Soc Aust 1944, 4, 119–131. [Google Scholar]
  212. Dudgeon, J.A. Congenital rubella. J Pediatr 1975, 87, 1078–1086. [Google Scholar] [CrossRef]
  213. Reddy, A.K.; Renganathan, S.N.; Jayamohan, A.E.; Lakshmanan, P.M. Gregg syndrome aka embryopathia rubeolaris: CT illustration. BMJ Case Rep 2014, 2014, bcr2014204204. [Google Scholar] [CrossRef]
  214. Kanai, M.; Kamiya, H.; Okuno, H.; et al. Epidemiological characteristics of congenital rubella syndrome cases during rubella epidemic in Japan, 2012-2014. Open Forum Infect Dis 2017, 4, S243. [Google Scholar] [CrossRef][Green Version]
  215. Begum, N.N.F. Novel facial characteristics in congenital rubella syndrome: A study of 115 cases in a cardiac hospital of Bangladesh. BMJ Paediatr Open 2020, 4, e000860. [Google Scholar] [CrossRef]
  216. De Santis, M.; Cavaliere, A.F.; Straface, G.; Caruso, A. Rubella infection in pregnancy. Reprod Toxicol 2006, 21, 390–398. [Google Scholar] [CrossRef]
  217. Plotkin, S.A. Rubella eradication: Not yet accomplished, but entirely feasible. J Infect Dis 2021, 224, S360–S366. [Google Scholar] [CrossRef] [PubMed]
  218. Yazigi, A.; De Pecoulas, A.E.; Vauloup-Fellous, C.; Grangeot-Keros, L.; Ayoubi, J.M.; Picone, O. Fetal and neonatal abnormalities due to congenital rubella syndrome: A review of literature. J Matern Fetal Neonatal Med 2017, 30, 274–278. [Google Scholar] [CrossRef]
  219. Frenkel, L.D.; Gomez, F.; Sabahi, F. The pathogenesis of microcephaly resulting from congenital infections: Why is my baby’s head so small? Eur J Clin Microbiol Infect Dis 2018, 37, 209–226. [Google Scholar] [CrossRef]
  220. Adams Waldorf, K.M.; McAdams, R.M. Influence of infection during pregnancy on fetal development. Reproduction 2013, 146, R151–R162. [Google Scholar] [CrossRef] [PubMed]
  221. Centers for Disease Control and Prevention (CDC). Three cases of congenital rubella syndrome in the postelimination era–Maryland, Alabama, and Illinois, 2012. MMWR Morb Mortal Wkly Rep 2013, 62, 226–229. [Google Scholar]
  222. Lambert, S.R. Congenital rubella syndrome: The end is in sight. Br J Ophthalmol 2007, 91, 1418–1419. [Google Scholar] [CrossRef] [PubMed]
  223. Mawson, A.R.; Croft, A.M. Rubella virus infection, the congenital rubella syndrome, and the link to autism. Int J Environ Res Public Health 2019, 16, 3543. [Google Scholar] [CrossRef]
  224. Paramita, D.V.; Purnami, N. Profile of congenital rubella syndrome in Soetomo General Hospital Surabaya, Indonesia. Infect Dis Rep 2020, 12, 8718. [Google Scholar] [CrossRef] [PubMed]
  225. Hall, R.E. The medicolegal aspects of abortion. Obstet Gynecol Annu 1972, 1, 339–350. [Google Scholar] [PubMed]
  226. Barnes, A.C. Rubella, abortion, and the law. Arch Otolaryngol 1973, 98, 275–276. [Google Scholar] [CrossRef]
  227. Carabali, M.; Harper, S.; Lima Neto, A.S.; et al. Spatiotemporal distribution and socioeconomic disparities of dengue, chikungunya and Zika in two Latin American cities from 2007 to 2017. Trop Med Int Health 2021, 26, 301–315. [Google Scholar] [CrossRef] [PubMed]
  228. Kreitzer, R.J.; Smith, C.W.; Kane, K.A.; Saunders, T.M. Affordable but inaccessible? contraception deserts in the US States. J Health Polit Policy Law 2021, 46, 277–304. [Google Scholar] [CrossRef] [PubMed]
  229. Nikpour, G.; Allen, A.; Rafie, S.; Sim, M.; Rible, R.; Chen, A. Pharmacy implementation of a new law allowing year-long hormonal contraception supplies. Pharmacy (Basel) 2020, 8, 165. [Google Scholar] [CrossRef]
  230. Kroelinger, C.D.; Romero, L.; Lathrop, E.; et al. Meeting summary: State and local implementation strategies for increasing access to contraception during Zika preparedness and response - United States, September 2016. MMWR Morb Mortal Wkly Rep 2017, 66, 1230–1235. [Google Scholar] [CrossRef]
  231. Barber, J.S.; Ela, E.; Gatny, H.; et al. Contraceptive desert? Black-white differences in characteristics of nearby pharmacies. J Racial Ethn Health Disparities 2019, 6, 719–732. [Google Scholar] [CrossRef]
  232. Okwori, G.; Smith, M.G.; Beatty, K.; Khoury, A.; Ventura, L.; Hale, N. Geographic differences in contraception provision and utilization among federally funded family planning clinics in South Carolina and Alabama. J Rural Health 2022, 38, 639–649. [Google Scholar] [CrossRef]
  233. Ambrogi, I.G.; Brito, L.; Diniz, D. The vulnerabilities of lives: Zika, women and children in Alagoas State, Brazil. Cad Saude Publica 2021, 36, e00032020. [Google Scholar] [CrossRef]
  234. Malta, M.; Murray, L.; da Silva, C.M.F.P.; Strathdee, S.A. Coronavirus in Brazil: The heavy weight of inequality and unsound leadership. EClinicalMedicine 2020, 25, 100472. [Google Scholar] [CrossRef]
  235. Stein, R.A.; Ometa, O. When public health crises collide: Social disparities and COVID-19. Int J Clin Pract 2020, 74, e13524. [Google Scholar] [CrossRef]
  236. Wenham, C.; Smith, J.; Davies, S.E.; et al. Women are most affected by pandemics - lessons from past outbreaks. Nature 2020, 583, 194–198. [Google Scholar] [CrossRef] [PubMed]
  237. Qiao, L.; Martelli, C.M.T.; Raja, A.I.; et al. Epidemic preparedness: Prenatal Zika virus screening during the next epidemic. BMJ Glob Health 2021, 6, e005332. [Google Scholar] [CrossRef] [PubMed]
  238. Pielnaa, P.; Al-Saadawe, M.; Saro, A.; et al. Zika virus-spread, epidemiology, genome, transmission cycle, clinical manifestation, associated challenges, vaccine and antiviral drug development. Virology 2020, 543, 34–42. [Google Scholar] [CrossRef] [PubMed]
  239. Rabionet, S.E.; Zorrilla, C.D.; Rivera-Viñas, J.I.; Guerra-Sanchez, Y. Pregnancy and Zika: The quest for quality care and reproductive justice. P R Health Sci J 2018, 37, S45–s50. [Google Scholar]
  240. Forero-Martínez, L.J.; Murad, R.; Calderón-Jaramillo, M.; Rivillas-García, J.C. Zika and women’s sexual and reproductive health: Critical first steps to understand the role of gender in the Colombian epidemic. Int J Gynaecol Obstet 2020, 148 (Suppl. 2), 15–19. [Google Scholar] [CrossRef]
  241. Ventura, D.; Rached, D.; Martins, J.; Pereira, C.; Trivellato, P.; Guerra, L. A rights-based approach to public health emergencies: The case of the ‘More Rights, Less Zika’ campaign in Brazil. Glob Public Health 2021, 16, 1576–1589. [Google Scholar] [CrossRef]
  242. McGovern, T.; Schaaf, M.; Battistini, E.; Maistrellis, E.; Gibb, K.; Casey, S.E. From bad to worse: Global governance of abortion and the Global Gag Rule. Sex Reprod Health Matters 2020, 28, 1794411. [Google Scholar] [CrossRef]
  243. Aiken, A.R.A. Erosion of women’s reproductive rights in the United States. BMJ 2019, 366, l4444. [Google Scholar] [CrossRef]
  244. The Lancet. The erosion of women’s sexual and reproductive rights. Lancet 2019, 393, 1773. [Google Scholar] [CrossRef]
  245. Parker, W.J. The moral imperative of reproductive rights, health, and justice. Best Pract Res Clin Obstet Gynaecol 2020, 62, 3–10. [Google Scholar] [CrossRef]
  246. McCullough, L.B.; Coverdale, J.H.; Chervenak, F.A. Professional ethics in obstetrics and gynecology, 1st ed.; Cambridge University Press, 2019. [Google Scholar] [CrossRef]
  247. The American College of Obstetricians and Gynecologists. Abortion is essential health care. 2022. Available online: https://www.acog.org/advocacy/abortion-is-essential (accessed on 8 July 2022).
  248. Boorman, J.P.; Porterfield, J.S. A simple technique for infection of mosquitoes with viruses; transmission of Zika virus. Trans R Soc Trop Med Hyg 1956, 50, 238–242. [Google Scholar] [CrossRef] [PubMed]
  249. Marchette, N.J.; Garcia, R.; Rudnick, A. Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia. Am J Trop Med Hyg 1969, 18, 411–415. [Google Scholar] [CrossRef]
  250. Lanciotti, R.S.; Kosoy, O.L.; Laven, J.J.; et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 2008, 14, 1232–1239. [Google Scholar] [CrossRef]
  251. Foy, B.D.; Kobylinski, K.C.; Chilson Foy, J.L.; et al. Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg Infect Dis 2011, 17, 880–882. [Google Scholar] [CrossRef] [PubMed]
  252. Oehler, E.; Watrin, L.; Larre, P.; et al. Zika virus infection complicated by Guillain-Barre syndrome–case report, French Polynesia, December 2013. Euro Surveill 2014, 19, 20720. [Google Scholar] [CrossRef] [PubMed]
  253. Cao-Lormeau, V.M.; Roche, C.; Teissier, A.; et al. Zika virus, French polynesia, South pacific, 2013. Emerg Infect Dis 2014, 20, 1085–1086. [Google Scholar] [CrossRef]
  254. Cao-Lormeau, V.M.; Blake, A.; Mons, S.; et al. Guillain-Barré syndrome outbreak associated with Zika virus infection in French Polynesia: A case-control study. Lancet 2016, 387, 1531–1539. [Google Scholar] [CrossRef]
  255. Musso, D.; Bossin, H.; Mallet, H.P.; et al. Zika virus in French Polynesia 2013-14: Anatomy of a completed outbreak. Lancet Infect Dis 2018, 18, e172–e182. [Google Scholar] [CrossRef] [PubMed]
  256. Faria, N.R.; Azevedo, R.D.S.D.S.; Kraemer, M.U.G.; et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science 2016, 352, 345–349. [Google Scholar] [CrossRef]
  257. Teixeira, M.G.; Costa Mda, C.; de Oliveira, W.K.; Nunes, M.L.; Rodrigues, L.C. The epidemic of Zika virus-related microcephaly in Brazil: Detection, control, etiology, and future scenarios. Am J Public Health 2016, 106, 601–605. [Google Scholar] [CrossRef]
  258. Fellner, C. Zika in America: The year in review. P T 2016, 41, 778–791. [Google Scholar]
  259. McCarthy, M. First US case of Zika virus infection is identified in Texas. BMJ 2016, 352, i212. [Google Scholar] [CrossRef][Green Version]
  260. Likos, A.; Griffin, I.; Bingham, A.M.; et al. Local mosquito-borne transmission of Zika virus - Miami-Dade and Broward Counties, Florida, June-August 2016. MMWR Morb Mortal Wkly Rep 2016, 65, 1032–1038. [Google Scholar] [CrossRef]
  261. Ventura, C.V.; Albini, T.A.; Berrocal, A.M. First locally transmitted Zika virus cases identified in the United States. JAMA Ophthalmol 2016, 134, 1219–1220. [Google Scholar] [CrossRef]
  262. Mallhi, T.H.; Khan, Y.H.; Tanveer, N.; Khan, A.H.; Bukhsh, A. Zika in India and the need for transparent reporting. Travel Med Infect Dis 2017, 18, 75–76. [Google Scholar] [CrossRef] [PubMed]
  263. Bispo, A. Brazil’s scientists scramble to solve the Zika puzzle. Bull World Health Organ 2016, 94, 165–166. [Google Scholar] [CrossRef] [PubMed]
Table 1. Key events in the history of the Zika virus. Data are based on references [4,7,9,10,11,12,13,20,21,22,30,35,38,39,67,68,248,249,250,251,252,253,254,255,256,257,258,259,260,261,262,263].
Table 1. Key events in the history of the Zika virus. Data are based on references [4,7,9,10,11,12,13,20,21,22,30,35,38,39,67,68,248,249,250,251,252,253,254,255,256,257,258,259,260,261,262,263].
YearEvent
April 1947 The first isolation of the Zika virus from a febrile sentinel rhesus monkey in Uganda
January 1948 The first isolation of the Zika virus from Aedes africanus mosquitoes
1956 The first demonstration that the Zika virus replicates in Aedes aegypti mosquitoes
1964 The first report of Zika virus infection in humans in Uganda
1966 The first isolation of the Zika virus from Aedes aegypti mosquitoes outside of Africa, in Malaysia
2007 The beginning of the Zika virus outbreak on Yap Island, the Western Pacific
2008 The first report of human-to-human transmission through intercourse
2013 The first report of Guillain-Barré syndrome (GBS) after an infection with the Zika virus
2013-2014 The Zika virus outbreak from French Polynesia
early 2014 The first confirmation of local transmission of the Zika virus in the Americas on Easter Island, Chile
early 2015 Detection of the Zika virus in Brazil
October 2015 The complete Zika virus genome was recovered from a fetus with microcephaly, in a woman who returned from Brazil to Slovenia
late 2015 Description of microcephaly in Brazil
Detection of Zika virus RNA in the amniotic fluid of pregnant women with fetal microcephaly
December 2015 First local transmission of the Zika virus in a US jurisdiction, in Puerto Rico
February 2016 The WHO declares Zika a Public Health Emergency of International Concern (PHEIC)
February 2016 The first sexual transmission of the Zika virus in the US, from a traveler who returned from Venezuela to Texas
July 2016 The first recognized outbreak of mosquito-borne transmission of Zika virus in the continental US in a neighborhood from Miami-Dade County, Florida
November 2016 The first instance of locally transmitted Zika in Texas
2016 The first link between Zika virus and the acute motor axonal neuropathy variant of GBS supported by clinical and electrodiagnostic evidence
2016 The first laboratory cases of Zika virus infection reported in India
2017-2021 Zika virus reported in 16 states/union territories from India

Share and Cite

MDPI and ACS Style

Stein, R.A.; Grayon, A.; Katz, A.; Chervenak, F.A. The Zika Virus: An Opportunity to Revisit Reproductive Health Needs and Disparities. Germs 2022, 12, 519-537. https://doi.org/10.18683/germs.2022.1357

AMA Style

Stein RA, Grayon A, Katz A, Chervenak FA. The Zika Virus: An Opportunity to Revisit Reproductive Health Needs and Disparities. Germs. 2022; 12(4):519-537. https://doi.org/10.18683/germs.2022.1357

Chicago/Turabian Style

Stein, Richard A., Alexis Grayon, Adi Katz, and Frank A. Chervenak. 2022. "The Zika Virus: An Opportunity to Revisit Reproductive Health Needs and Disparities" Germs 12, no. 4: 519-537. https://doi.org/10.18683/germs.2022.1357

APA Style

Stein, R. A., Grayon, A., Katz, A., & Chervenak, F. A. (2022). The Zika Virus: An Opportunity to Revisit Reproductive Health Needs and Disparities. Germs, 12(4), 519-537. https://doi.org/10.18683/germs.2022.1357

Article Metrics

Back to TopTop