Correlated prevalence of hydrocele and microfilaremia in Amazon (Belém, 1951-2005)

Dilma Costa de Oliveira Neves; Habib Fraiha-Neto; Ana de Nazaré Martins da Silva; Yara Lúcia Lins Jennings; Ana Paula Martins da Silva; Cristina Nunes; Roberta Nice Sodré; Cláudio Eduardo Corrêa Teixeira

doi:10.4103/0972-9062.321756

RESEARCH ARTICLE

Year : 2021 | Volume : 58 | Issue : 3 | Page : 240-245

Correlated prevalence of hydrocele and microfilaremia in Amazon (Belém, 1951-2005)

Dilma Costa de Oliveira Neves¹, Habib Fraiha-Neto², Ana de Nazaré Martins da Silva², Yara Lúcia Lins Jennings², Ana Paula Martins da Silva², Cristina Nunes², Roberta Nice Sodré², Cláudio Eduardo Corrêa Teixeira³
¹ Centro Universitário do Estado do Pará, Av. Almirante Barroso, 3775 - Souza - 66013-903 - Belém; Universidade Federal do Pará, Núcleo de Medicina Tropical, Av. Generalíssimo Deodoro, 92 – Umarizal - 66055-240 - Belém, Pará, Brazil
² Universidade Federal do Pará, Núcleo de Medicina Tropical, Av. Generalíssimo Deodoro, 92 – Umarizal - 66055-240 - Belém, Pará, Brazil
³ Centro Universitário do Estado do Pará, Av. Almirante Barroso, 3775 - Souza - 66013-903 - Belém, Pará, Brazil

Date of Submission	13-Dec-2019
Date of Acceptance	07-Aug-2020
Date of Web Publication	15-Feb-2022

Correspondence Address:
Cláudio Eduardo Corrêa Teixeira
Centro Universitário do Estado do Pará, Av. Almirante Barroso, 3775 - Souza - 66013-903 - Belém, Pará
Brazil

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/0972-9062.321756

Abstract

Background & objectives: For decades, the city of Belém in Brazil’s eastern Amazon was the second city in the country with highest prevalence of cases of filariasis due to Wuchereria bancrofti infection. However, this prevalence decreased over time until reaching null records, concomitantly with a decrease in frequency of recorded hydrocele cases. In this context, we analyzed cross-sectional data to evaluate the degree of correlation between prevalence of positive blood microfilariae results during surveillance screening occurred along 54 years (1951–2005) and prevalence of hydrocele cases recorded in the same time period.
Methods: The dataset regarding hydrocele cases was obtained from two local hospitals. The Endemic Diseases Control Division of the Health Surveillance Department of the Municipal Health Department of Belém provided dataset regarding positive blood microfilariae cases. Prevalence calculus and linear correlation statistics were performed.
Results: Both positive blood microfilariae and hydrocele cases are well correlated statistically in absolute frequency (r = 0.871, 95%_CI = 0.788 to 0.923, R² = 0.759, p < 0.0001) and in prevalence (r = 0.835, 95%_CI = 0.732 to 0.901, R² = 0.698, p < 0.0001).
Interpretation & conclusion: We have concluded that blood microfilariae detection and hospitalized hydrocele cases are well correlated in our dataset. In addition, these results support the hypothesis that hydrocele prevalence can be useful to filariasis surveillance and control in endemic areas. However, limitations to hydrocele prevalence as an epidemiological indicator of filariasis are evidenced.

Keywords: Lymphatic filariasis; Scrotal hydrocele; Filaria bancrofti

How to cite this article:
de Oliveira Neves DC, Fraiha-Neto H, Martins da Silva Ad, Lins Jennings YL, Martins da Silva AP, Nunes C, Sodré RN, Corrêa Teixeira CE. Correlated prevalence of hydrocele and microfilaremia in Amazon (Belém, 1951-2005). J Vector Borne Dis 2021;58:240-5

How to cite this URL:
de Oliveira Neves DC, Fraiha-Neto H, Martins da Silva Ad, Lins Jennings YL, Martins da Silva AP, Nunes C, Sodré RN, Corrêa Teixeira CE. Correlated prevalence of hydrocele and microfilaremia in Amazon (Belém, 1951-2005). J Vector Borne Dis [serial online] 2021 [cited 2023 Mar 29];58:240-5. Available from: http://www.jvbd.org//text.asp?2021/58/3/240/321756

Introduction

Wuchereria bancrofti is a worm that impedes lymphatic vessels drainage, causing lymphatic filariasis^[1]. In male, intrascrotal lymphatic vessels also are affected, a condition called hydrocele^{[2],[3],[4],[5]}. The use of the prevalence of hydrocele as a diagnostic index to obtain rapid, reliable and valid estimates of lymphatic filariasis burden in a given community has been proposed^[6]. However, as hydrocele is restricted to male patients and can also be caused by conditions other than lymphatic filariasis, its potential as a reliable epidemiological indicator of filariasis occurrence becomes controversial. With the aim of helping clarify this issue, in this study we investigated the degree of correlation between the historical series (1951–2005) of positive blood microfilariae cases detected in the city of Belém (Brazil) and the frequency of hospitalized hydrocele cases at hospitals of the same city in the same period.

The city of Belém, capital of the State of Pará, located in the eastern Amazon region of northern Brazil, was considered the second city with the largest number of cases of lymphatic filariasis in Brazil for more than three decades, being the most epidemiologically relevant in Brazilian Amazon^[7]. Studies from 1940 to 1950 showed filariasis prevalence of 10.8% in Belém, characterizing this city as an endemic area^[8] During the National Lymphatic Filariasis Campaign (1951–1958), Belém was ranked as the second Brazilian city with largest prevalence of filariasis (9.8%)^[9]. Even with a national strategy to decrease filariasis incidence through treatment of individually diagnosed patients with diethylcarbamazine and vector control, Belém remained as one of the two Brazilian capitals still considered as active areas of transmission in the decades that followed^[10],[11]. However, as a result of control intervention implemented, prevalence of filariasis consistently decreased over the 1990s and 2000s, until evidencing the interruption of transmission in Belém, in 2005.

Several studies have supported the eradication of filariasis in Belém. For instance, after dissection of a large number of females of Culex quinquefasciatus carried out in 2002 and 2003, none was found to be infected with W. bancrofti^[12]. In addition, circulating filarial antigen surveys among 3,000 school children (6–10 years old) in 2002, and among 2816 young adult males (20–30 years old) in 2005, both resulted in negative results^[13]. In general, these results confirmed the lack of active transmission of W. bancrofti in Belém until 2005. Unfortunately, since then no new large survey has been conducted to update this information, despite a consensus that knowledge about current situation is essential to prevent emergence of new foci and/or reemergence of filariasis in regions where it has been eliminated.

In this context, we analyzed whether or not there is a relevant degree of correlation between prevalence of hydrocele and microfilaremia in a 54 years surveillance historical series, contributing to clarify if a growing occurrence of hydrocele could indicate an insidious reemergence of filariasis in endemic regions as cities of Brazilian Amazon.

Material & Methods

Dataset regarding frequency of hydrocele cases was obtained from two local hospitals (Hospital da Fundação Santa Casa de Misericórdia do Pará and Hospital Beneficente Portuguesa D. Luiz I), where almost all patients with hydrocele in Belém received medical care in the period from 1951 to 2005. In this study we have included solely dataof patients that were living in Belém in this time period and aged 10 years or older. Although exposure to infecting larvae is expected to occur early in childhood in endemic areas^[14], there is evidence that the chronic form of the disease rarely occurs in children younger than 10 years^[15],[16]. Duplicate records were eliminated from the dataset analysis based on patients’ name, age, origin, address, date of hospital admission, and/or medical records’ number. On the other hand, dataset regarding the frequency of positive blood microfilariae cases during the same time period was provided by the Endemic Diseases Control Division of the Health Surveillance Department of the Municipal Health Department of Belém, without record of sex and age of patients.

Prevalence of both hydrocele and positive blood microfilariae cases from 1951 to 2005 were calculated based on the total population of Belém during each year. The Endemic Diseases Control Division of the Health Surveillance Department of the Municipal Health Department of Belém provided dataset about total population of Belém from 1951 to 1959, while the Department of Informatics of the Unified Health System of the Ministry of Health/ Brazil provided the dataset referring to total population of Belém from 1960 to 2005, based on census data of the Brazilian Institute of Geography and Statistics.

Data analysis to evaluate the degree of correlation between variables under study was performed using Pearson’s linear correlation coefficient (r), coefficient of determination (R²), t test for linear correlation coefficients (∝ = 0.05), and 95% confidence intervals for linear correlation coefficients, all calculated using GraphPad Prism version 7 for Mac (GraphPad Software, La Jolla California USA; www.graphpad.com).

Ethical statement

This work was approved by the Research Ethics Committee of the Tropical Medicine Nucleus of the Federal University of Pará under protocol number 123/2005- CEP/NMT, in accordance with the Helsinki Declaration.

Results

The absolute frequencies of total population of Belém and of population sample tested for blood microfilariae along 54 years (1951–2005) are shown in [Figure 1]A. It is noted that population sampling achieved a peak between 1970–1980, but decreased thereafter. [Figure 1]B also shows the absolute frequencies of population sample tested for blood microfilariae and of positive blood microfilariae cases from each year sample along the same period. This provides evidence that the decrease in population sampling between 1970–1980 and thereafter occurred in parallel to a strong decrease in detection of positive blood microfilariae cases along each year of sampling.

Figure 1: Absolute frequencies of the total population of the city of Belém (A, black circles), of population sample tested for blood microfilariae (A and B, blue circles), and of positive blood microfilariae cases (B, red circles) from each year sampling along 54 years.

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In addition, it is possible to observe in [Figure 2]A that, while the total population of the city of Belém increased over the years, the absolute frequencies of both positive blood microfilariae cases and hospitalized hydrocele cases decreased along the time period under study. This simultaneous decrease both in frequencies of positive blood microfilariae and hydrocele cases is well correlated statistically (r =0.871, 95%_CI = 0.788 to 0.923, R² = 0.759, p< 0.0001) [Figure 2]C. Similarly, [Figure 2]B shows that a decrease in prevalence of positive blood microfilariae cases occurs concomitantly with a decrease in prevalence of hospitalized hydrocele cases along the same period, wherein both the prevalence of positive blood microfilariae cases and hospitalized hydrocele cases are also well correlated statistically (r = 0.835, 95%_CI = 0.732 to 0.901, R² = 0.698, p< 0.0001) [Figure 2]D. However, it is worth noting that along more than 4 decades (1951–1996) the number of cases of positive blood microfilariae were much larger than the number of hydrocele hospitalized cases [Figure 3]. In addition, [Figure 4] shows that most patients hospitalized with hydrocele along the time period under study are between 20–30 years old, with a prominent decrease in frequency of cases with ages below and above this range.

Figure 2: A. Absolute frequencies of the total population of Belém (black circles), of positive blood microfilariae (red circles), and of hydrocele cases (green circles) along 54 years. B: Prevalence of positive blood microfilariae (red circles) and of hydrocele cases (green circles) along 54 years. C: Dispersion diagram correlating absolute frequencies of positive blood microfilariae and of hydrocele cases. D: Dispersion diagram correlating prevalence of positive blood microfilariae and of hydrocele cases. Diagonal dotted line illustrates a perfect statistical correlation.

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Figure 3: Difference between absolute frequencies of positive blood microfilariae cases and of hospitalized hydrocele cases along 54 years (1951-2005).

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Figure 4: Absolute frequency of hospitalized hydrocele cases as a function of age of patients hospitalized along 54 years (1951-2005).

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Discussion

The degree of correlation between hydrocele records and positive blood microfilariae showed in the present work is quantitatively similar to that observed in Ghana^[6]. However, this correlation might be even stronger if we had separated male and female datasets of positive blood microfilariae available. In addition, the prevalence of hydrocele in the population of Belém might have been yet higher than that observed in the data collected from the hospitals’ records. Along the years both hospitals from where data about hydrocele were collected underwent fire and some data certainly were lost in these incidents.

Hydrocele is considered the most common manifestation of lymphatic filariasis in endemic areas^[17], and therefore a strong correlation between hydrocele and microfilaremia prevalence was expected. Indeed, many studies indicate a positive correlation between hydrocele and filariasis^{[18],[19],[20]}, although some studies show such correlation as not evident^[21],[22] or inconclusive^[23]. And based on this evidenced correlation, it has been proposed that hydrocele prevalence is a good predictor of filariasis burden in a given community^[6]. The present dataset supports the herein hypothesis that the frequency of hydrocele cases can be useful to infer filariasis burden in a given community, although this approach seems to be of limited power for that purpose.

Such a limitation must be attributed to many factors. For example, in the present work it is possible to observe that, although strongly correlated in frequency and prevalence, the number of cases of positive blood microfilariae is significantly larger than that of hospitalized hydrocele cases. Although hydrocele prevalence is consensually considered high among male patients with filariasis^[24], not all infected male patients develop hydrocele. Thus, if in an outbreak of filariasis a significant number of patients infected are female or are male that do not develop hydrocele, the prediction power of the correlation between filariasis and hydrocele cases proves to be weak. On the other hand, it cannot be disregarded that in Amazon region many patients might have difficulties to access medical care or just do not seek medical care. Therefore, if these patients are not included in official records of filariasis and hydrocele, although fewer in number, their absence should weaken even further the power of hydrocele record as an epidemiological indicator of filariasis.

Finally, the age profile of hydrocele patients showed in the present work is inconsistent with those of cross- sectional clinical trials conducted in India^[25] and in Kenya^[26], which show an increase in hydrocele cases with age and a higher prevalence of this morbidity in men over 40 years. Indeed, it has been shown that microfilariae are observed in chronic lymphatic filariasis when there is hydrocele^{[27],[28],[29],[30]}. One could hypothesize that such age differences are due to the fact that most hydrocele cases have asymptomatic profile, and this postpones diagnosis in countries where healthcare services are not easily available and/or cultural aspects constraint the search for healthcare. In contrast, the fact that most patients hospitalized with hydrocele in our dataset were at young adult age range, this might reflect longevity of family careful even with their young adult individuals, a strong characteristic of Latin populations. Thus, the power of hydrocele prevalence in predicting filariasis burden in a given community might be constrained by age-related susceptibility, healthcare access and availability, as well as efficient passive surveillance.

Currently, transmission of lymphatic filariasis in Brazil is officially restricted to endemic areas in North East of the country, belonging to municipalities of the State of Pernambuco. Between 2008 and 2013, 516 cases were registered positive, with Olinda presenting 48.6% (n = 251) of the cases; Recife, 23.1% (n = 119); Jaboatão dos Guararapes, 24.4% (n = 126); and Paulista, 3.9% (n = 20). Although notification is compulsory, there was no record of new cases in the period from 2014 to 2016. In such endemic areas, passive surveillance and periodic surveys with blood collection every two years and treatment of positive cases are expected. In non-endemic areas, passive surveillance with treatment of positive cases and home and neighborhood investigation are expected^[31]. Therefore, as the results of the present work highlight hydrocele as a potential indicator of microfilariasis, mainly among young adults, this should be emphasized in passive surveillance, contributing to filariasis eradication in this country until 2022, as aimed.

Conclusion

We have concluded that there is a relevant statistical correlation between the prevalence of positive blood microfilariae and hydrocele in the historical dataset of surveillance in Belém. This supports the hypothesis that hydrocele prevalence might be a potential indicator of filariasis burden in endemic regions. However, the same dataset indicate that this power of prediction is probably limited by a number of factors (age-related susceptibility to hydrocele, healthcare access and availability, efficient passive surveillance of filariasis, in addition to vector- parasite-host interactions and the quality of surveillance recordings). Thus, future studies should investigate which factors constrain this power of prediction and how much such constrains limit this approach.

Conflict of interest: None

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