Expansion of Zika virus circulation from Africa to the Americas, 1947

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Narrative

review

Expansion of Zika virus circulation from Africa to the

Americas, 1947-2018: a literature review*

Correspondence:

Gilmara de Souza Sampaio – Universidade Federal da Bahia, Hospital Universitário Edgard Santos, Laboratório de Pesquisa em

Infectologia, Rua João das Botas, No. 157b, Canela, Salvador, BA, Brazil. Postcode: 40110-160

E-mail: gilmara.s[email protected]

Gilmara de Souza Sampaio

– orcid.org/0000-0001-7299-3740

Carlos Brites

– orcid.org/0000-0002-4673-6991

Jan Felix Drexler

– orcid.org/0000-0002-3509-0232

Andres Moreira-Soto

– orcid.org/0000-0002-9224-5157

Fernanda Miranda

– orcid.org/0000-0002-7654-6443

Eduardo Martins Netto

– orcid.org/0000-0003-1691-6761

Universidade Federal da Bahia, Hospital Universitário Professor Edgard Santos, Salvador, BA, Brasil

Charité – Universitätsmedizin Berlin, Institut für Virologie, Berlim, Alemanha

Abstract

Objective: to describe the temporal and geographical expansion of Zika virus (ZIKV) circulation in countries and territories,

from the time it was ﬁrst isolated until 2018. Methods: This was a non-systematic literature review covering the period from

1947 to 2018 using the MEDLINE database and World Health Organization estimates. Results: Since its isolation in 1947,

ZIKV circulation spread through Africa, Asia and the Paciﬁc before reaching the Americas in 2013, causing serious clinical

manifestations; the highest seroprevalence rates were recorded in Yap (74%) and in Brazil (63%); genetic mutations, absence

of immunity and high vector susceptibility may have inﬂuenced ZIKV transmissibility and help to explain the magnitude of its

expansion. Conclusion: The spread of ZIKV circulation in the Americas was the most extensive recorded thus far, possibly

as a result of population and geographical characteristics of the sites where the virus circulated.

Keywords: Zika Virus, Flavivirus; Epidemiology; Epidemics; Congenital Abnormalities; Review Literature as Topic.

doi: 10.5123/S1679-49742019000200022

*Article derived from the Ph.D. dissertation entitled ‘The spread, prevalence and dynamics of Zika virus transmission, 1947-2018’,

defended by Gilmara de Souza Sampaio at the Health Sciences Postgraduate Program, Faculty of Medicine, Federal University of

Bahia, on March 21

2019.

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Expansion of Zika virus circulation: from Africa to the Americas

Introduction

Following its discovery in 1947, Zika virus (ZIKV) was

responsible for sporadic cases of mild infections that

were not cause for great concern and were limited to the

African and Asian continents.

This scenario changed with

effect from 2007, when the virus began to be considered

a pathogen capable of causing large epidemics after

having produced two large-scale outbreaks in the Paciﬁc

Islands

2-4

and in French Polynesia.

4-6

ZIKV circulation

continued to expand (Figure 1A). Within a short time,

the virus was considered to be a Public Health concern

associated with a large number of microcephaly cases

that occurred in Brazil.

7,8

Concern as to the severity of the consequences of

infection led the Ministry of Health to declare a state

of Public Health Emergency of National Concern on

November 11

2015.

Following this declaration, the

Pan American Health Organization (PAHO) issued an

alert about the increased number of microcephaly cases

in Brazil’s Northeast region.

Just days afterwards, on

November 28

2015, despite there being little evidence,

the Ministry of Health conﬁrmed the link between

ZIKV and the microcephaly outbreak.

On December

2015, the World Health Organization (WHO) and

PAHO issued an alert suggesting possible association

between ZIKV and the increase in cases of congenital

syndrome and Guillain-Barré syndrome.

On February

2016, WHO declared a Public Health Emergency of

International Concern.

The agility with which health

authorities and researchers acted enabled rapid proof

of the causal relationship between ZIKV infection and

the occurrence of microcephaly and other central

nervous system alterations. This position was endorsed

by WHO at a meeting of the Emergency Committee held

in June 2016

(Figure 1B).

The potential of the virus to give rise to a broad

spectrum of clinical manifestations was conﬁrmed,

ranging from non-specific symptoms, easily

confused with other virus diseases, to neurological

manifestations and congenital malformations.

7,8,15-19

By the end of 2016, 2,366 Zika virus-associated

congenital abnormalities had been confirmed in

Brazil.

The emergence of ZIKV in the Americas and

the potential for its circulation to expand require better

comprehension of its epidemiological proﬁle, in order

to facilitate understanding of the changes in infection

detected over time.

The objective of this literature review was to

describe the temporal and geographic expansion of

KIKV circulation in countries and territories, from the

time it was isolated up until 2018.

Methods

This is a narrative review of ZIKV circulation

expansion over the years in countries and territories

on diverse continents. We searched the MEDLINE

database (via PubMed), using the following keywords

retrieved from the Health Sciences Descriptors (DeCS)

virtual library: ‘zika’, ‘zika virus’, ‘flavivirus’ and

‘arbovirus’. Eligible articles were those that provided

microbiological evidence of ZIKV infection in humans

and non-humans published between 1947 and 2018, in

any region of the world, and which contained complete

information on how the study was conducted: period,

place, sample, type of test used for diagnosis and test

result. We excluded articles that did not present positive

laboratory test results for the virus in humans or where

virus isolation in non-humans was not conducted. No

restriction was made as to language or whether the

publication was free of charge or not.

We also used estimates, available on the ofﬁcial

website of the PAHO-WHO, of conﬁrmed Zika cases or

conﬁrmed cases of Zika infection-associated congenital

syndrome, occurring in countries or territories in

the Americas up until January 2018.

In order to

demonstrate the magnitude of infection in different

places, ZIKA infection seroprevalence in the samples

examined was calculated as follows: ﬁrstly we totaled the

positive test results and then divided the total number

of tests by the total number of samples in each study.

Global expansion of ZIKV circulation

1940s and 1950s

ZIKV is believed to have emerged in around

1920,

although it was only isolated in 1947 in a

study on yellow feber in Rhesus monkeys conducted

by researchers from the Virus Research Institute.

The term ‘Zika’ was borrowed from the name of the

By the end of 2016, 2,366 Zika virus-

associated congenital abnormalities

had been conﬁrmed in Brazil.

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Gilmara de Souza Sampaio et al.

Emergence of the virus

around 1920

Virus isolated

in Aedes

First records of infection

on the Asian continent,

in Malaysia

Emergence of the virus

in the Paciﬁc, on the

Micronesian island of Yap

Emergence of the virus on the

American continent

Records of Guillain-Barré

syndrome and microcephaly

cases

Virus isolated in rhesus

monkeys un Uganda

First cases of human

infection recorded

in Africa

First cases of infection by

Aedes aegypti recorded

in Malaysia

Virus emerges in French

Polynesia

Records of Guillain-Barré

syndrome cases

Ministry of Health declares

Public Health Emergency of

National Concern

Ministry of Health conﬁrms

relationship between Zika

virus and microcephaly

WHO declares Public

Health Emergency of

International Concern

WHO declares end of

Public Health Emergency

of International Concern

PAHO issues alert about

increased microcephaly cases in

Northeast Brazil

WHO issues alert about possible

association between Zika

Virus and increased number of

microcephaly and Guillain-Barré

syndrome cases

WHO conﬁrms association

between Zika virus and

microcephaly

Ministry of Health declares end

of Public Health Emergency of

National Concern

Notes:

A) Timeline of Zika virus circulation expansion up until 2015.

B) Measures adopted by health authorities (Brazilian Ministry of Health, Pan American Health Organization [PAHO] and World Health Organization [WHO]) in the face of the increased number of

microcephaly Guillain-Barré syndrome cases in Brazil.

Figure 1 – Timeline of Zika virus circulation expansion and measures adopted by health authorities

Zika forest, in Entebbe, Uganda, where the Institute

was based. Despite the study mentioned above being

focused on yellow feber and dengue, researchers found

evidence of Zika virus being a new pathogen.

In 1948, less than a year after its discovery, ZIKV was

isolated in the Aedes (Stegomyia) africanus vector,

22-24

even though at that time it was not known that it was

a ZIKV vector.

ZIKV spread following its original lineage, referred

to as African lineage Zika, and expanded over part

of the African continent.

In West Africa it was

introduced twice, at different times, and gave origin

to two African lineages.

The ﬁrst human ZIKV infections were recorded in

1952, on the African continent, and were conﬁrmed

by its presence in serum of ZIKA neutralizing

antibodies.

25,26

At that time there was no other way of

demonstrating ZIKV infection, since test results could

be biased because of a possible immune response

to yellow feber vaccination.

During the 1950s,

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Expansion of Zika virus circulation: from Africa to the Americas

studies identiﬁed the presence of these antibodies in

people living in North Africa,

West Africa,

25,28

East

Africa

22,26,29,30

and Central Africa,

as well as in South

Asia

and Southeast Asia

27,32-34

(Figure 2 and Figure

3A). The highest seroprevalence rates were recorded

in Malaysia and the Philippines: 50% and 36%,

respectively (Table 1).

Jaundice was found in the three human cases

identiﬁed in 1954, indicating that the virus could also

be viscerotropic.

Another characteristics described

was its afﬁnity for nerve tissues, found in mice that

developed neurological diseases after being infected.

Aedes aegypti was found to be a ZIKV vector in 1956.

1960s to 1990s

The third ZIKV lineage, i.e. the Asian lineage,

originated from a strain isolated in Malaysia in around

1966.

It was here that the ﬁrst Zika virus infection

attributed to the Aedes aegypti vector was recorded.

At that time, serological and virological evidence

indicated that it was circulating in almost all of Africa,

in its Northern,

39,40

Central,

40-43

Western

40,44-48

and

Eastern regions

39,49,50

(Figure 2 and Figure 3B). The

majority of the countries in these regions are located

in latitudes where the climate is tropical and this is

propitious for vector development. Joint circulation

of yellow feber virus and Zika virus was found in a

region of Ethiopia in 1968.

Studies indicate that ZIKV

antibodies can attenuate yellow feber virus infection

but do not interfere with its transmission.

51,52

In the

decades in question, the highest seroprevalence rates

were recorded in Burkina Faso (53%), Mali (52%)

and Benin (44%).

2000s

For more than half a century, ZIKV remained

conﬁned to the African and Asian continents, before

emerging in the Paciﬁc Islands in the late 2000s.

Between April and July 2007, the ﬁrst large epidemic

caused by the virus occurred in Yap, an island in

Micronesia (Figure 2). Infection incidence was high

in this outbreak at around 74% (95% conﬁdence

interval: 68-77).

Despite affecting the majority of

the population, only around 20% of total cases were

symptomatic and reported mainly having exanthema,

conjunctivitis and pain in their joints.

2,3

The serum

samples of the inhabitants of Yap were tested by means

of the enzyme-linked immunosorbent assay (ELISA),

the virus neutralization test to detect antibodies (NT)

and reverse transcription polymerase chain reaction

(RT-PCR). Phylogenetic analyses showed that a strain

of the Asian lineage of the virus was responsible for

this outbreak.

By the end of the 2000s, ZIKV had been isolated

in Ae. Aegypti, Ae. africanus, Ae. apicoargenteus,

Ae. luteocephalus, Ae. vitattus, Ae. Furcifer and Ae.

Hensilii species vectors,

36,38,48,51,53

whereby the latter

was the most frequent species in the Yap outbreak.

For a long time it was believed that the only form of

Zika virus transmission was by the bite of mosquitoes

of the Aedes genus.

2,23,29,38,53

In 2008, however, two

researchers were infected in Senegal and one of them

transmitted ZIKV to his wife, possibly through sexual

intercourse.

Other studies have corroborated this

hypothesis by indicating the possibility of this form

of transmission.

55,56

2010s

The 2010s were marked by important discoveries,

such as the possibility of mother-to-child Zika

virus transmission and clinical manifestations with

unprecedented association with Zika virus infection,

such as congenital abnormalities

17,57,58

and Guillain-

Barré syndrome.

5,15,16

At that time the virus caused a new epidemic that

affected a considerable part of the population of French

Polynesia with effect from 2013, with approximately

thirty thousand people infected

5,6,59

and 42 patients

with Guillain-Barré syndrome.

15,16

That epidemic was

the consequence of a new strain that appeared in the

same year and was genetically related to the strains

isolated in Yap in 2007 and in Cambodia in 2010.

4,6

is likely that its magnitude was the result of a population

with low levels of immunity, high vector density

and

genetic mutations in which important amino acids

were modiﬁed, increasing the capacity of Zika virus

transmission by the Aedes aegypti vector.

ZIKV continued to expand to other Paciﬁc Ocean

Islands

4,5,59,61-64

and through Southeast Asia,

65-72

until

it was identiﬁed in the Americas in May 2015.

73-75

Between 2015 and 2016, seroprevalence in Brazil was

63% (Table 1).

The timeline of Zika virus circulation expansion is

shown in Figure 1A, while its geographic expansion is

shown in Figure 3, highlighted by period to demonstrate

its swiftness and extent.

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Gilmara de Souza Sampaio et al.

Continent/

region/year

Country or territory Type of test used

Continent/

region/year

Country or territory Type of test used

1940s 1970s

Africa Africa

1947 Uganda

IV 1972 Serra Leoa

132

1948 Uganda

1970-1972 Nigéria

53,128,133,134

NT, FC, HI

1950s 1971-1972 Angola

135

Africa

1972 e 1975 Senegal

1951 Nigéria

TPR 1976 Sudão

136

NT, HI

1952 Uganda

NT 1979 República Centro-Africana

137

1952 Tanzânia

NT Asia

1953 Nigéria

NT 1970-1979 Indonésia

129,130

1954 Chade

1970-1979 Paquistão

131

1954 Congo

NT 1980s

1954 Egito

Africa

1955 Nigéria

TPR 1980 Nigéria

138

1957 Moçambique

NT 1984 Uganda

139

1958 Uganda

1988 Senegal

ELISA

1960s Asia

Africa

1980-1983 Indonésia

129,130

1960 Angola

1980-1983 Paquistão

131

1961–1962 República Centro-Africana

HI 1990s

1961–1964 Etiópia

Africa

1962 Senegal

HI 1990-1991 Senegal

ELISA

1963–1964 República Centro-Africana

125

HI 1991-1992 Djibouti

ELISA

1963–1964 Burkina Faso

HI 1999 Costa do Marﬁm

ELISA

1963–1965 Costa do Marﬁm

126

HI Asia

1963–1965 Guiné-Bissau

1996-1997 Malásia

141

1964–1966 Togo

HI 2000s

1964-1966 Camarões

Oceania

1964-1967 Mali

HI 2007 Ilha de Yap, Micronésia

ELISA, RT-PCR

1965 Níger

HI Africa

1967 Libéria

2008 Senegal

NT, FC, HI

1967 Benin

HI 2010s

1967 Gabão

Oceania

1966-1967 Uganda

HI 2013-2014 Ilha de Páscoa

RT-PCR

1966-1967 Quênia

HI 2013-2014 Ilhas Cook

ELISA, RT-PCR

1966-1967 Somália

HI 2013-2014 Nova Caledônia

RT-PCR

1966-1967 Marrocos

HI 2011-2014 Polinésia Francesa

4,5,59

ELISA

1967-1969 Uganda

HI 2015 Fiji

RT-PCR

1968 Quênia

127

HI 2015 Samoa

RT-PCR

1969 Nigéria

128

NT Africa

Asia 2010 Camarões

142

FC, HI

1969 Malásia

IV 2014 Zâmbia

143,144

ELISA

1969-1983 Indonésia

129,130

2015 Cabo Verde

145

ELISA, RT-PCR

1969-1983 Paquistão

131

Legend:

NT: virus neutralization test to detect antibodies.

ELISA: enzyme-linked immunosorbent assay.

CF: complement ﬁxation test.

HI: hemagglutination inhibition test.

IMT: intracerebrally inoculated mice test.

VI: virus isolation.

PCR: polymerase chain reaction.

RT-PCR: reverse transcription polymerase chain reaction.

Figure 2 – Countries or territories recording Zika virus circulation between 1947 and 2018, listed by continent and

decade of occurrence

Continued on next page

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Expansion of Zika virus circulation: from Africa to the Americas

The seroprevalence tests used in the various

studies we consulted differ as to the method of

laboratory diagnosis used and, therefore, have

differing levels of sensitivity and speciﬁcity,

76,77

thus

compromising the comparability of the results of the

different methods applied.

RT-PCR was used in 31 studies and was the most

used test, followed by the hemagglutination inhibition

test (HI) in 24 studies, ELISA in 17 studies, NT in 13

studies and the complement ﬁxation test (CF) in 4

studies. Some studies used more than one diagnosis

method. Cross-reactivity between ZIKV antibodies and

those of other ﬂaviviruses may also have compromised

correct estimation of infection prevalence.

78,79

ZIKV in the Americas

The ﬁrst genetic studies of the strain causing the

ZIKV epidemic on the American continent suggest that

it originated from a unique Asian genotype lineage,

introduced in Brazil between late 2013 and early 2014

and having come from French Polynesia.

6,80-83

Four

hypotheses have been raised regarding the introduction

Continent/

region/year

Country or territory Type of test used

Continent/

region/year

Country or territory Type of test used

2010s 2010s

Asia North America

2010-2015 Camboja

PCR 2016-2017 Belize

2010-2015 Indonésia

66,67

RT-PCR, PCR 2016-2017 Bonaire, Santo Eustáquio e Saba

2010-2015 Malásia

ELISA, PCR 2016-2017 Costa Rica

2010-2015 Filipinas

ELISA, RT-PCR 2016-2017 Cuba

2010-2015 Maldivas

RT-PCR 2016-2017 Granada

2012-2014 Tailândia

71,72

RT-PCR 2016-2017 Guadalupe

21,155

RT-PCR

North America 2016-2017 Ilhas Cayman

2015-2017 México

21,146

ELISA, RT-PCR 2016-2017 Ilhas Virgens (US)

2016-2017 Estados Unidos

21,147

NT, ELISA, RT-PCR 2016 Ilhas Virgens (UK)

Central American and Caribbean 2016-2017 Jamaica

2014-2016 Haiti

21,148

RT-PCR 2016-2017 Nicarágua

21,156

RT-PCR

2015-2016 Guiana

2016-2017 República Dominicana

21,157

ELISA, RT-PCR

2015-2016 Martinica

21,149

RT-PCR 2016-2017 San Martin

2015-2017 Barbados

21,150

RT-PCR 2016-2017 San Martin (parte holandesa)

2015-2017 Curaçao

2016 Santa Lúcia

2015-2017 El Salvador

2016 São Bartolomeu

2015-2017 Guatemala

2016-2017 São Cristóvão e Nevis

2015-2017 Panamá

21,151

ELISA, RT-PCR 2016 São Vicente e Granadinas

2015-2017 Guiana Francesa

2016-2017 Trindade e Tobago

2015-2017 Honduras

ELISA, RT-PCR 2016-2017 Ilhas Turcas e Caicos

2015-2017 Porto Rico

21,152

ELISA, RT-PCR South America

2015-2017 Suriname

21,153

RT-PCR 2015-2017 Brasil

21,73–75

RT-PCR

2016 Antígua e Barbuda

2015-2017 Colômbia

21,158

RT-PCR

2016 Dominica

21,154

RT-PCR 2015-2017 Venezuela

52,106

RT-PCR

2016 Guiné-Bissau

2016-2017 Argentina

2016 Montserrat

2016 Bolívia

21,159

NT, ELISA

2016-2017 Anguila

2016-2017 Equador

21,160

RT-PCR

2016-2017 Aruba

2015-2017 Paraguai

2016 Bahamas

2016-2017 Peru

21,161

RT-PCR

Legend:

NT: virus neutralization test to detect antibodies.

ELISA: enzyme-linked immunosorbent assay.

CF: complement ﬁxation test.

HI: hemagglutination inhibition test.

IMT: intracerebrally inoculated mice test.

VI: virus isolation.

PCR: polymerase chain reaction.

RT-PCR: reverse transcription polymerase chain reaction.

Figure 2 – Countries or territories recording Zika virus circulation between 1947 and 2018, listed by continent and

decade of occurrence

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Gilmara de Souza Sampaio et al.

of the virus in Brazil. Initially it was thought that it

had happened in 2014, during the FIFA World Cup,

despite there being no Paciﬁc countries among the

participating soccer teams. A second possibility was

that the virus was introduced during the Canoe Sprint

World Championship, held in August 2014 in Rio

de Janeiro, as there were teams from four Paciﬁc

countries with registered Zika cases: French Polynesia,

New Caledonia, the Cook Islands and Easter Island.

However, the hypothesis of the virus having entered

Brazil via Rio de Janeiro does not help to explain why

such a high number of cases were concentrated in the

country’s Northeast region. The third hypothesis is that

the virus was introduced one year earlier, between July

and August 2013, during the Confederations Cup.

According to the fourth and ﬁnal hypothesis, the virus

circulated in Oceania and Easter Island, spreading to

Central America and the Caribbean before arriving in

Brazil at the end of that year.

The only ancestor of

the cases studied was a strain from Haiti, indicating

that ZIKV could have been introduced in Brazil by

immigrants or Brazilian troops returning from that

country. However, recent studies indicate that the

virus followed a different route, namely from Brazil to

Central America, entering via Honduras, between July

and September 2014.

Phylogeographic analysis has

estimated that the virus arrived in Honduras from Brazil

and later spread to Guatemala, Nicaragua and southern

Mexico by early 2015. Another study corroborates

the hypothesis that the introduction of ZIKV in South

America occurred prior to its introduction in Central

America, possibly in the ﬁrst half of 2013.

In Outober 2014, some municipalities of the

Brazilian states of Rio Grande do Norte, Paraíba and

Maranhão reported suspected cases of a viral disease

with presence of exanthema, mild feber, itching and

painful joints, these being symptoms not in keeping

with suspected cases of other exanthematous viral

infections, such as measles and dengue. Before long

a further six states reported exanthematous syndrome

cases between October 2014 and March 2015.

The intense and concomitant circulation of other

ﬂaviviruses, together with similar clinical presentation,

low speciﬁcity of ELISA diagnostic tests for dengue

well as the fact of the presence of the pathogen in Brazil

still being unknown, led to ZIKV not being indicated

as the main suspect.

In March 2015, samples from the states of Rio

Grande do Norte and Bahia had positive ZIKV results

conﬁrmed by RT-PCR.

73,74

It spread well beyond Brazil’s

borders. By late 2015, ten Central and Southern

American countries had recorded autochthonous

Dec. 2010

Dec. 2000

Dec. 60 a 90

Dec. 50

Uganda

No cases reported

1:275.207.309 1:275.207.309

Notes:

A) Countries or territories registering Zika virus circulation by the 1950s.

B) Countries or territories registering Zika virus circulation during the 1960s, 1970s, 1980s and 1990s.

C) Countries or territories registering Zika virus circulation in the 2000s; the circle indicates the Paciﬁc Islands.

D) All countries recording presence of Zika virus between 2010 and January 2018.

Figure 3 – Geographic and temporal expansion of Zika virus

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Expansion of Zika virus circulation: from Africa to the Americas

Table 1 – Zika virus seroprevalence in humans by affected country and period of infection, 1947-2016

Period Country/reference Type of test used No. of cases Total

Seroprevalence

(%)

1947-1984

Uganda

23,26,39,127,139

IMT, NT, HI 56 798 7

1947-1952 Tanzânia

IMT 6 36 17

1951-1975

Nigéria

25,28,40,53,128,132,138

NT,IMT,HI 1,090 3,018 36

1952 Índia

NT 33 196 17

1953 Filipinas

NT 19 53 36

1953, 1954 Malásia

27,33

NT 90 179 50

1954 Tailândia

NT 8 50 16

1954 Vietnã

NT 2 50 4

1954 Egito

NT 1 180 1

1957 Moçambique

NT 10 149 7

1960-1972

Angola

41,135

HI 202 5,082 4

1961-1979

República Centro-Africana

42,125

HI 186 1,177 16

1961-1964 Etiópia

HI 48 1,316 4

1962-1990

Senegal

44,46,47

HI, ELISA 203 1,292 16

1963,1964 Burkina Faso

HI 1,005 1,896 53

1963-1999

Costa do Marﬁm

48,126

HI, ELISA 393 906 43

1964,1965 Guiné-Bissau

HI 122 1,054 12

1964-1966 Togo

HI 401 1,294 31

1964-2010

Camarões

43,142

HI, CF 626 3,714 17

1964-1967 Mali

HI 1,232 2,369 52

1965 Níger

HI 55 308 18

1966 Somália

HI 3 242 1

1966-1968 Quênia

50,127

HI 509 3,134 16

1967 Benin

HI 108 244 44

1967 Gabão

HI 50 717 7

1972 Serra Leoa

132

HI 62 899 7

1983 Paquistão

131

CF 1 43 2

1983 Indonésia

129,130

HI 9 71 13

2007 Ilha de Yap, Micronésia

ELISA 414 557 74

2011-2013

Polinésia Francesa

ELISA 319 1,069 30

2014 Zâmbia

144

ELISA 217 3,625 6

2015-2016 Brasil

123

ELISA, PRNT 401 633 63

a) 1947-1952, 1966, 1967, 1984.

b) 1951-1952, 1955, 1965, 1966, 1967, 1969-1971, 1971-1975, 1972.

c) 1960, 1971, 1972.

d) 1961, 1962, 1963, 1964, 1979.

e) 1962, 1988, 1990.

f) 1963-1965, 1999.

g) 1964-1966, 2010.

h) 2011-2013, 2014.

Legend:

NT: virus neutralization test to detect antibodies.

ELISA: enzyme-linked immunosorbent assay.

CF: complement ﬁxation test.

HI: hemagglutination inhibition test.

IMT: intracerebrally inoculated mice test.

PRNT: plaque reduction neutralization test.

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Gilmara de Souza Sampaio et al.

cases,

and by the beginning of the next year this

number had increased rapidly to 48 countries

88,89

(Figure 2 and Figure 3D). Only Canada and Bermuda,

both located in North America, and Chile and Uruguay,

in South America, did not have autochthonous cases.

Figure 4 shows the geographic and temporal spread

of ZIKV in the Americas, from the ﬁrst recorded case

on the continent up until 2017.

Of all these countries, Brazil had the highest number

of ZIKV infections, totaling 137,288 conﬁrmed cases

between 2015 and January 2018, followed by Puerto

Rico and Mexico, with 40,562 and 11,805 conﬁrmed

cases, respectively.

In 2016 the total number of

cases reduced by more than 95% compared to the

previous year and on November 18

2016 WHO

stopped considering the virus as a Public Health

Emergency of International Concern.

In May 2017,

the Brazilian Health Ministry also declared the end of

the emergency.

In the ﬁrst semester of 2015, a change was noted

in the pattern of the occurrence of Guillain-Barré

syndrome in two states of Brazil’s Northeast region,

namely Pernambuco and Bahia: in the former state

the number of cases tripled compared to the previous

year, with a peak in April, while Bahia recorded

a peak in occurrence of the syndrome between

June and July.

92,93

In the same period, four patients

undergoing solid organ transplantation were infected

with ZIKV, diagnosed by RT-PCR between June 2015

and January 2016.

In October of the same year, a

change was detected in the epidemiological pattern

of microcephaly occurrence, when Pernambuco state

health authorities informed the Ministry of Health about

a signiﬁcant increase in the number of cases.

In late

November 2015, the Evandro Chagas Institute in the

state of Pará, a body linked to the Health Ministry’s

Health Surveillance Secretariat (IEC/SVS/MS), sent the

result of tests performed on a baby with microcephaly

to the Ministry: presence of ZIKV in blood and tissues.

This resulted in the Ministry of Health conﬁrming the

relationship between ZIKV and microcephaly.

By the end of 2016, 22 countries had registered

cases of congenital syndrome associated with ZIKV

infection: a total of 2,525 reported cases, 2,289 (90%)

of which related to Brazil.

By December 2017, the 27

Brazilian states together recorded 3,071 microcephaly

cases, 2,004 (65%) of which occurred in the Northeast

region.

This number reduced signiﬁcantly to 123

new cases between January and May 2018. In all,

there was a total of 3,194 records possibly associated

with ZIKV infection since these began to be counted

in 2015.

Zika virus, the cause of this pandemic,

had become a potential Public Health threat owing to

its association with neurological complications and

congenital malformations, which have been widely

documented.

7,8,12,18,19

The epidemics caused by the virus brought to light

a broad range of clinical manifestations; although it is

not possible to know the magnitude of the complications

related to ZIKV infection, which may possibly be greater

than those found so far. Little is known about issues such

as the severity of clinical presentation of ZIKV infection

or its viral load, nor about its inﬂuence on the clinical

spectrum found in different places and populations.

A descriptive study

100

assessed 1,950 conﬁrmed

microcephaly cases in Brazil, 1,373 of which were

in the country’s Northeast region, using secondary

data obtained from the Health Ministry’s Notiﬁable

Diseases Information System (SINAN) relating to the

period between January 1

2015 and November 12

2016. Its results revealed two waves of ZIKV infection:

during the ﬁrst wave, in 2015, there was a monthly

peak of microcephaly occurrence estimated at 50

cases per 10,000 live births, most of them (70% of the

total) living in the Northeast region; during the second

wave, occurrence was much lower, with monthly peaks

estimated as varying between 3 and 15 cases per 10,000

live births. The number of microcephaly cases related

to ZIKV infection following both outbreaks, or waves,

showed temporal variation according to the region of

the country; the reasons for these differences have,

however, yet to be enlightened.

A possible explanation for the result of these

estimates is the fact that, during the second wave

of infection, the relationship between ZKV infection

and the microcephaly cases in question was already

suspected and even supported by evidence, leading

the government to broadcast campaigns with the aim

of keeping the population informed. Pregnant women

began to take prevention measures in order to avoid

contact with the vector, such as using insect repellent,

bug screens and even delaying planned pregnancy.

100

Little is known about genetic variations between

ZIKV lineages and their ability to interfere with ZIKV

pathogenicity.

101

One experimental study that used

trophoblasts derived from human embryonic stem

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Expansion of Zika virus circulation: from Africa to the Americas

1:180.934.416 1:180.934.416 1:180.934.416

2014-2015

2016

2017

No cases reported

A B C

Notes:

A) Countries or territories registering Zika virus circulation between 2014 and 2015.

B) Countries or territories registering Zika virus circulation in 2016.

C) Countries or territories registering Zika virus circulation in 2017.

Figure 4 – Geographic and temporal expansion of Zika virus in the Americas, 2015- 2017

cells, found differences between the African and Asian

lineages with regard to their behavior in the placenta.

The occurrence of cell lysis – the process through

which a cell is destroyed or dissolved by plasma

membrane rupture – was only found in infections by

the African ZIKV lineage; however, no differences were

found in virus replication rates in relation to infection

caused by the two strains. This characteristic supports

the deduction that infection by an African strain at

the beginning of pregnancy would probably result in

miscarriage rather than congenital malformations.

102

It is possible that ZIKV’s pathogenic potential

depends on individual genetic variations, as indicated

by a comparative experimental study of three pairs of

dizygotic twins, when only one of each pair of twins

was diagnosed as having ZIKV congenital syndrome.

The study found that after infecting neural tissues, the

virus caused delayed development of the cells of the

twins who had the syndrome as well as increasing virus

replication. Transcriptome analysis results showed

a significant difference in DDIT4L mTOR protein

inhibitor levels between twins that had the syndrome

and twins that did not. The results found suggest the

existence of a relationship between individual genetic

disposition and increase in mTOR signaling and,

given that mTOR signaling pathways are critical for

autophagy mediated virus puriﬁcation, ZIKV infections

are intensiﬁed in these people.

103

Discussion

The factors that led to large-scale and rapid

emergence, spread and apparent increase in Zika

virus pathogenicity in the Paciﬁc and the Americas

are not yet totally understood. It is possible that there

are various mechanisms in operation, including virus

mutations that might increase transmission from

humans to mosquitoes, modulating the host immune

response.

104-107

Another factor lacking explanation is

the absence of large epidemics in Africa and Asia. A

hypothesis given for this fact is that it possibly reﬂects

higher levels of immunity provided by cross-protection

against other ZIKV-related ﬂaviviruses ZIKV,

104

or that

epidemics that in fact existed may have been associated

with dengue due to the clinical similarity between

the two viruses dengue and due to their antibody

cross-reactivity.

37,108

Another study corroborated the

hypothesis that large outbreaks have not happened

in Africa because Aedes aegypti of African origin

may be less susceptible to virus strains than Aedes

aegypti that is not of African origin. Notwithstanding,

this characteristic has not helped to explain why there

have not been large outbreaks in Asia, different to the

Americas, given that the populations of both regions

had similar levels of susceptibility.

109

Intensity of ZIKV dissemination, viremia and clinical

symptoms in the Americas, including microcephaly,

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Gilmara de Souza Sampaio et al.

could have intensiﬁed owing to dengue virus immunity

existing in endemic regions.

110

However, a pediatric

cohort study conducted in Nicaragua between January

and February 2017 monitored 3,700 children aged

2 to 14 years and concluded that the opposite may

occur, i.e. ZIKV infection symptoms may be reduced

owing to prior dengue virus immunization.

111

This

hypothesis is corroborated by research involving an

experiment with mice that demonstrated the effect

of dengue infection on CD8+ T-cells in guaranteeing

cross-protection against ZIKV during pregnancy.

112

Another factor capable of intensifying dissemination

was a slight genetic alteration in ZIKV polyprotein

which happened before the 2013 outbreak and was

sufﬁcient to permanently increase its infectivity in

human nerve cells.

105

This fact would help to explain

why microcephaly cases have been so numerous in the

Americas in comparison to other continents.

Other aspects to be considered are related to

Aedes aegypti and Aedes albopictus susceptibility, as

well as that of ZIKV strains, due to genetic differences

that inﬂuence vector response levels to infection and

consequent ZIKV transmission capacity.

113-120

The

American strain is more easily transmitted than the

Asian strain from which it is derived, this being an

hypothesis conﬁrmed by analysis of vector saliva: only

the virus in the sample containing the American strain

remained viable after three days of infection, in addition

to having a higher infection rate in Aedes aegypti.

121

The highest number of Zika and microcephaly

cases was recorded in Northeast Brazil. Some reasons

indicated for this were presented in an ecological

analysis study: joint circulation of the virus that causes

Chikungunya feber, which exists in this region, could

increase the risk of other communicable diseases

being transmitted.

122

Another study found higher ZIKA

prevalence infection in poorer social classes.

123

The

fact that the ﬁrst notiﬁcations of infections occurred in

Northeast Brazil, along with the massive media alerts

that followed, helped measures to be taken that may

possibly have contained greater spread of the virus in

other regions. The same reasoning could be applied to

Brazil, where the ﬁrst infections were recorded, and to

the other Latin American countries where cases were

not numerous.

The Brazilian epidemic showed a sharp decline in

recorded infections with effect from 2017. A possible

cause of this may have been high seroprevalence in

the population, leading to immunity against ZIKV.

123,124

A study conducted in Bahia, a Northeastern Brazilian

state, assessed 633 individuals based on their serum

samples collected between 2015 and 2016. The

results of the analyses showed a rapid increase in ZIKV

infection seroprevalence in the population, reaching

63% in 2016.

123

It is possible that population and

geographic characteristics may have directly inﬂuenced

the pace of propagation, and the possible reasons

for this would be the variations in vector density,

immunity and changes in routine habits, as well as

high population mobility.

100,120,123

The outbreak in the Americas has ended.

Notwithstanding, a study supported by a stochastic

spatial model has indicated the possibility of the

emergence of new epidemics approximately every ten

years, this being the time needed for a new generation

of the population to become susceptible once more.

124

In conclusion, the spread of ZIKV circulation

seen in the last decade was the swiftest and largest

recorded thus far. Possible factors contributing to this

include genetic changes that increased its transmission

potential, together with favorable population and

geographic characteristics in the regions where the virus

circulated. Large numbers of microcephaly cases were

expected to occur in most countries in the Americas,

but in the end this expectation was not conﬁrmed.

Similarly, the reasons why Brazil recorded such a higher

number of cases in comparison to other Latin American

countries has not been totally explained. Nor have the

reasons why most of the infections recorded in Brazil

were concentrated in its Northeastern region. This gives

rise to several unanswered questions as to increased

virus circulation and pathogenicity. Another limitation

of this literature review relates to the different methods

adopted in the studies consulted, thus hindering precise

seroprevalence rates from being obtained. Cross-

reactivity, caused by other ﬂavivirus antibodies, was

a limiting impediment to the accuracy of the results

presented.

Further research is needed to overcome gaps in

knowledge about ZIKV pathogenesis and to assess

local risks; seroprevalence studies to identify regions

vulnerable to infection so as to foresee the potential

of future epidemics. A beneﬁt of this work is that the

efforts of health authorities would be better directed,

so as to contribute to the development of effective Zika

virus infection control measures.

Epidemiol. Serv. Saude, Brasília, 28(2):e2018411, 2019

Expansion of Zika virus circulation: from Africa to the Americas

Vaccine development also needs to be encouraged,

in order to interrupt the transmission chain and avoid

future outbreaks and epidemics.

Acknowledgement

We thank the Brazilian Hospital Services Company

(EBSERH), for its support in the development of

this study.

Authors’ contributions

Netto EM, Sampaio GS, Brites C, Moreira-Soto A and

Drexler JF took part in the conception and planning of the

study and writing and critical revision of the manuscript

contents. Sampaio GS and Miranda FL collected and

analyzed the study data. All the authors approved the

version to be published and take on responsibility for all

aspects of the work, including its accuracy and integrity.

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Received on 04/02/2019

Approved on 17/04/2019

Associate editor: Taís Freire Galvão – orcid.org/0000-0003-2072-4834