Arboviruses represent a global risk for more than 80% of the planet's population. Chikungunya virus causes epidemics characterized by explosive outbreaks in geographical areas interspersed with periods of disappearance that can last for years or decades. This study sought to outline the epidemiological aspects of Chikungunya fever (CHIKF) in the state of Rio Grande do Norte, using as a guiding source the primary data obtained from samples processed and analysed at LADIC.
In 2019, the most positive samples for CHIKV occurred in March in Natal; the same month with the highest occurrence of cases observed in the year 2020, when most of the analysed samples were from the interior of the state (Fig. 1). In 2019, the rainfall peak occurred at the beginning of April (Embrapa 2021). Thus, it is inferred that the incidence of cases in Natal is unrelated to increased rainfall. This result is in line with what was observed by Monteiro et al., (2020). In contrast, in the 2020 analysis, the cases in Guamaré – the municipality with the most positive samples (17/33%) and which occurred entirely in March, were proceeded by heavy regional rains (Embrapa 2021).
The highest number of confirmed cases in females (59.7%) corroborates the findings of Duncan et al., (2017) and Monteiro et al., (2020) (Online Resource 4). The more significant occurrence of cases in women can be justified by the higher presence in the domestic and peridomicile environment and, therefore, greater exposure to vectors (Vasconcelos et al. 1993). In addition, it is recognized that seeking health services behaviour is more common among women. Elderlies between 60 and 70 years of age or older represent 22% (2019) and 19% (2020) of infections (Online Resource 5). It has been shown that in this group age, the impact of clinical symptoms is more significant and in people of more advanced age, especially in those with poor health, the disease can be lethal (Thiboutot et al. 2010). The most cited sign among both genders was fever (64.9%). Other common signs and symptoms were: headache (47.76%), arthralgia (47.01%) and myalgia (41.04%) (Online Resource 6). In a study by Bloch et al., (2016), these manifestations tended to be significantly associated with laboratory-confirmed cases of CHIKF.
In our sample, there were three newborns among the individuals who had a confirmed diagnosis of CHIKF. Two of the correspondent mothers were tested. The mothers aged between 21 and 39, fit into the most frequent age group found in the study (Online Resource 5). The time of symptomatology in both mothers (FV509 = 8 days; FV932 = 4 days) was longer than the lifetime of their newborn children (FV510 = 7 days; FV931 = 1 day), respectively. This finding suggests the occurrence of congenital chikungunya in at least two of the three newborns cause by vertical transmission from mother to child, which is the occurrence of symptoms during the first week of life, in the absence of evidence that their newborns had been exposed to mosquito bites (Torres et al. 2016). Inferring the time elapsed from the clinical signs of infection, the onset of symptoms in the newborn FV510 occurred on day 2 of life and in FV931 on day 1. These data contradict the findings obtained by Torres (2016), who in his work noted that 86% of newborns became ill on the fifth day after birth. As for the clinical signs reported in this group, they presented fever, exanthema, headache, back pain, arthritis, arthralgia, petechiae and retro-orbital pain. In addition to these signs and symptoms, studies include reports of dehydration, neurological and cardiac manifestations associated with this group during epidemic outbreaks(Barr and Vaidhyanathan 2019). It is important to emphasize that neurological sequelae can affect those patients who have encephalitis associated with chikungunya for a period that can extend from six months to two years (Robin et al. 2008; Gérardin et al. 2014). Thus, long-term clinical follow-up and neurological reassessment are essential for these neonatal patients, especially those affected by congenital CHIKF (Alvarado-Socarras et al. 2016).
Only one of the mothers (FV509) had CHIKF infection confirmed by qRT-PCR. Mother FV932 was not confirmed by qRT-PCR, despite having myalgia, headache, rash, back pain, arthritis, intense arthralgia, petechiae and retroorbital pain and a period of four days of symptoms, which is the ideal time to carry out viral detection. Various factors can interfere with the diagnostic outcome, from sample stability to low viral load or a failure of appropriate RNA extraction. In this case, a retest is recommended, or another test, such as immunological tests to detect anti-CHIKV IgM, is chosen.
Furthermore, two participants who did not show apparent symptoms of infection were positive in the test, which corresponded to 1.5% (2/143) of the total number of cases (Online Resource 7 and Online Resource 6). In population studies of epidemic areas, especially seroprevalence studies, the rate of asymptomatic patients shows considerable variability (Gay et al. 2016), whether in conglomerate or randomized model samples. However, it is believed that these cases, along with mild cases of infection, may have an important impact on the transmissibility of the virus (Bloch et al. 2016). From all observed samples, the highest mean viral load peak was found on the first day of symptom onset (Online Resource 8).
A variety of urban characteristics can be seen among Natal neighbourhoods that can promote the spread of arboviruses (da Silva and Barbosa 2020). The Tirol neighbourhood - where the highest proportion of cases was identified in 2020 - presents better socioeconomic conditions and sanitary infrastructure compared to other neighbourhoods, in addition to having sewage coverage and regular collection points for solid waste. However, Tirol is located adjacent to the Dunas Park Natal (Parque Nacional das Dunas), an ecological protection region integrated into the Atlantic Forest domain, where evidence of virus circulation was found in the mosquito species of Aedes fluviatilis, Ae. albopictus, Ae. aegypti and Wyeomyia bourrouli in 2019, which would have favoured the high frequency of Chikungunya cases in the neighbourhood (Ximenes et al. 2020). The confirmed cases in this study were collected during an outbreak, when residents of the neighbourhood, in a collective effort, screened probable cases. The increase in cases is attributed to the proliferation of vectors that reproduce inside numerous idle or abandoned properties, where the presence of accumulated garbage was observed associated with the proximity of Dunas Park Natal, where Ae. albopictus is abundant (Tribuna do Norte 2019; Ximenes et al. 2020).
Capim Macio neighbourhood shares characteristics like those of the Tirol neighbourhood, except that it has low sewage coverage (da Silva and Barbosa 2020). The neighbourhoods of Pajuçara, Lagoa Azul and Planalto, were among those with the highest number of cases in 2019. These neighbourhoods have lower monthly income per capita and solid waste accumulation points. Pajuçara and Lagoa Azul are in the North region, where the highest concentration of population and demographic density of the city is located. Planalto, which had the highest notification numbers in 2019, presents a population increase and a deficit in basic sanitation systems, which drives the spread of vectors.
From the positive samples collected in 2020, 49 of the participant specimens had their place of residence identified, belonging to 13 different municipalities. Most cases came from the city of Guamaré, corresponding to 33%. In Guamaré, the positive samples were distributed in the neighbourhoods of Vila Maria, the city Center and Salina da Cruz, all located in the urban area of the municipality, around a water reservoir structure that resembles a shrimp farm, as seen in (Online Resource 11 and 12). The municipality is recognized for its industrial activity of shrimp farming. Between 2015 and 2020, Guamaré presented an accumulated number of CHIKV notifications of just over 500 cases, according to the National Ministry of Health (SESAP-RN 2021), with a high incidence rate in 2016 and 2020. It is worthwhile to note that between 2014 and 2017, one of the highest incidences of dengue in the Northeast was attributed to this municipality (do Carmo et al. 2020), indicating that it had established conditions for the dissemination of other arboviruses.
The other municipalities had cases distributed in different parts of urban and peri-urban areas. Interestingly, four participants came from rural areas of the municipalities of Lajes, Parazinho and Nova Cruz. However, it is not possible to say whether these infections occurred in that environment. In any case, the mobility of infected individuals between these environments in proximity to the sylvatic cycle is striking, which can occasionally lead to the establishment of the virus in the enzootic cycle. Introducing the virus to the sylvatic cycle can give rise to points of re-emergence in the urban cycle, implying a severe impact on public health (Weaver 2013).
Water scarcity significantly impacts the living conditions of the population, favouring the spread of infectious diseases (Githeko et al. 2000; Alpino et al. 2016). The prevalent climate condition in Rio Grande do Norte favours inadequate water storage for domestic use that contributes to the formation of mosquito breeding sites, facilitating human contact with the vectors (Weaver and Reisen 2010). This fact is pointed out as one of the factors responsible for an outbreak of CHIKV in Kenya (Chretien et al. 2007). The endemicity of chikungunya in a population depends on the intensity of Ae. aegypti infestation in the environment. However, dense population pockets of these mosquitoes can keep CHIKV endemic at moderate levels (Halstead 2019). In Rio Grande do Norte, Ae. aegypti is the primary vector identified in the transmission of CHIKV; however, evidence of DENV (Medeiros et al. 2018) and CHIKV (Ximenes et al. 2020) was observed in Ae. albopictus, a generalist mosquito that adapts to varied environmental conditions in tropical and temperate areas, as well as to domestic and peri-domestic environments (Lambrechts et al. 2010). In conclusion, in this study, we characterize cases of CHIKF that occurred in the Potiguar territory and point out possible reasons for the continuous circulation of the virus in the state.