Abstract
This work was aimed at assessing the prevalence of paragonimiasis and crab-eating behavior in Southeastern Nigeria. Sputum examinations and questionnaire administration were carried out. Prevalence was 13.2% and was significantly higher among females (14.6%) than males (11.2%) (). Overall, 77.2% of respondents across the communities eat crabs, and this was comparable between males (76.4%) and females (77.6%) (). The prevalence was comparable between the two ethnocultural groups and between communities within each ethnocultural group ( for both tests). The mean age of crab eaters was 43 years, while that of noncrab eaters was 26 years. Many (46.3%) infected individuals presented low intensity infections (1–50 eggs/ova per 5 mL−1 sputum), while 28.8% and 23.8% presented moderate (51–100 eggs/ova per 5 mL−1 sputum) and high (above 100 eggs/ova per 5 mL−1 sputum) intensity infections, respectively. Infection risk among weekly eaters of crabs was 3 times higher than that of monthly eaters (OR 3.68), 19 times higher than that of quarterly eaters (OR 19.0), and 9 times higher than that of irregular eaters (OR 9.38). Concerted awareness campaign is needed to curb the renewed increase of the scourge in endemic Southeastern Nigeria.
1. Introduction
An estimated 22 million people are infected with paragonimiasis worldwide, and 10% of them live in Africa and Central and South America [1]. Paragonimiasis is one of the food-borne trematode (FBT) infections in humans, acquired following the consumption of raw or improperly cooked crabs or crayfish, containing infective metacercariae (cysts). According to Fried and Abruzzi [2], species of snail serve as the first intermediate host while local freshwater crustaceans (crabs and crayfish) serve as the second intermediate hosts, while humans and various mammals that feed on infected crustaceans are the definitive hosts of these lung flukes. In the host duodenum, the metacercariae excyst and penetrate the gut, and then the diaphragm, before migrating to the lung parenchyma. They develop into adult worms in cysts in the lungs. Here they lay eggs, which may be expectorated or swallowed and passed with stools, thus initiating a new cycle. The egg is an important diagnostic tool for detecting this trematode in the host, although other types of immunological and molecular detection tests are available [3].
Paragonimiasis is a neglected but reemerging zoonotic parasitic infection in Nigeria. It is now two and a half decades since endemic paragonimiasis was last reported in Southeastern Nigeria [4]. Endemic foci had been reported in Enugu and the areas around the Imo and Cross River, and their tributaries [5], Igwun River and River Iduma including Abam, Arochukwu, Bende, and Ohafia towns among others [4]. Our personal observations in some new foci in Eastern Nigeria have revealed massive eating of the crab species Sudanautes, which has been earlier confirmed as the intermediate host of Paragonimus uterobilateralis in Eastern Nigeria [4]. This work was therefore aimed at assessing the prevalence of paragonimiasis and crab-eating behavior among six communities in two main ethnocultural groups in Southeastern Nigeria. The specific objectives of the study include the following: (i) to ascertain the prevalence and intensities of vector infection in the six communities in Southeastern Nigeria; (ii) to determine the proportion of the population that eat crabs and how frequently they eat them; and (iii) to compare the results in (i) and (ii) above between the Igbo and Ikwerre ethnocultural groups that comprised the study area in Southeastern Nigeria.
2. Materials and Methods
2.1. The Study Areas
Six communities, comprising of three each from the two ethnocultural groups were studied in Southeastern Nigeria. The two main ethnocultural groups, were Ndi Igbo and Ikwerre groups. The three communities from the Ndi Igbo ethnocultural group were the Umulolo, Igwun River Basin, and Iduma River basin areas, which are located in the Imo River Basin, Igwun River Basin, and Iduma River Basin, respectively. These three communities are typically rural in setting and of monolithic population. They are mostly subsistent farmers, fishermen, artisans, traders, and significantly few white collar jobs. In these communities, crabs are caught by people in all categories of occupation for both subsistence and commercial purposes and sold both locally and in nearby towns. They are regarded as traditional delicacy.
The three study communities from the Ikwerre ethnocultural group were Oyigbo (located in the Imo River Basin), Choba, and Ogbakiri communities (both located in the New Calabar River Basin). These three communities are in the suburb of Port Harcourt, sprawling and highly populated and rapidly growing capital city of oil-rich Rivers State in the Niger Delta. Apart from the Ogbakiri that is rural in setting and of monolithic population, Choba and Oyigbo are urban and constituted predominantly of nonindigenes, and they could be described as assimilated into the Port Harcourt city. The population in these communities is constituted (in the reverse order to that of the Igbo ethnocultural communities) mostly of white collar jobbers, traders, artisans, fishermen, and lastly farmers. In these communities, crabs are caught by the indigenous Ikwerre people for both subsistence and economic purposes. The population here regards crab eating as delicacy to complement for both meat and fish as source of protein.
2.2. Studying Crab-Eating Behavior in the Study Area
All consenting persons from the study areas were helped to complete a structured questionnaire comprised of four questions bothering on personal biodata and on whether or not they did eat crabs. The questions were as follows: (1) Sex (male or female). (2) Age. (3) Do you eat crab? (yes or no). (4) How often do you eat crabs? (weekly, monthly, quarterly, yearly, or irregularly).
2.3. Examination for Paragonimus uterobilateralis
All consenting persons were provided with vials and asked to use them to provide their sputum. All the vials were collected from all consenting persons the following morning and brought to the laboratory. Sputum samples were examined for the presence of Paragonimus uterobilateralis eggs/ova to provide a diagnosis of paragonimiasis. To make up for the sensitivity concerns of sputum examination for detection of eggs, seven sputum examinations per person were carried out as recommended [1]. The estimated sensitivity, specificity, and positive and negative predictive values of sputum sampling in the area were calculated to be 0.60, 0.63, 0.13, and 0.97, respectively. All individuals found to have eggs in their sputum were treated with praziquantel at a dose of 3 × 25 mg/kg of body weight per day for 3 consecutive days [6].
2.4. Ethical Clearance
Ethical approval for the study was received from the Cross River University of Technology Ethical Committee. Additionally, ethical clearance was obtained from the Ministry of Health in the five respective Local Government Areas, which are the Bende LGA in Abia State, the Okigwe LGA in Imo State, and the Oyigbo, Obio/Akpor, and Emohua LGAs in Rivers State.
2.5. Data Analysis
The Epi Info version 6.0 was used in entering data, and SPSS for windows (1995 version) was used for data analysis. The geometric mean intensity (GMI) of eggs/ova was calculated as antilog , with being the egg/ova counts per 5 mL of sputum in infected individuals and the number of infected individuals examined. Proportions were compared by chi-square or Fisher’s exact test and relative risks of infection by odds ratio (OR).
3. Results
3.1. Prevalence of Human Infection
A total of 604 consenting individuals provided sputum samples in the study, comprising 242 (40.1%) males and 362 (59.9%) females. Of these 80 (13.2%) were found infected with P. uterobilateralis. The prevalence of infection was 11.2% (27) for men and 14.6% (53) for women, and the difference was significant . The prevalence of paragonimiasis among the communities ranged from 10.1% in Choba to 17.4% in Umulolo Okigwe (see Table 1), and there was no evidence of significant difference between the communities .
3.2. Assessment of Human Infection in relation to Crab Eating among Respondents
The distribution of prevalence of infection and the crab-eating behavior among the various communities is also shown in Table 1. Overall, 77.2% (466) of respondents across the various communities eat crabs, and this was comparable between males (; 76.4%) and females (; 77.6%) . Crab eating among the communities ranged from 66.9% in Oyigbo to 91.5% in Ogbakiri. The prevalence was comparable between both the two ethnocultural groups and between communities within each ethnocultural group ( for both tests).
The comparison between crab-eating and non-crab-eating categories showed that three-quarter of crab eaters were females (see Table 2). The mean age of crab eaters was 43 years, while that of noncrab eaters was 26 years.
3.3. Intensity of Infection
The frequency distribution of intensities of infection is summarized in Table 3. Egg counts of 1–50 eggs/ova per 5 mL−1 sputum, 51–100 eggs/ova per 5 mL−1 sputum, and above 100 eggs/ova per 5 mL−1 were regarded as low, moderate, and high intensities, respectively. Based on this categorization, 46.3% of infected individuals presented low intensity infections as against 28.8% and 23.8% who presented with moderate and high intensity infections, respectively.
3.4. Regularity of Crab Eating
The prevalence of paragonimiasis infection increased with increasing frequency of crab eating as shown in Table 4. The risk of paragonimiasis infection among those who ate crabs weekly was 3 times higher than among those who ate monthly (OR 3.68), 19 times higher than among those who ate quarterly (OR 19.0), and 9 times than among irregular eaters (OR 9.38). The risk of being infected among those who ate crabs irregularly was twice of those who ate crabs quarterly (OR 1.95).
4. Discussion
Paragonimus species are extremely successful parasites and are widely geographically distributed. They are found in tropical, subtropical, and temperate climates [7]. More recently, it has been estimated that 293 million people are at risk, whereas several million are actually infected [3, 8]. Geographic regions that have or have had a high prevalence of disease include Cameroon, which is contiguous to Southeastern Nigeria. However, environmental factors, such as pollution, adversely affect the population of either the first (freshwater snail) or second (freshwater crustacean) intermediate host and hence consequently affect the prevalence of the disease [7].
The prevalence of P. uterobilateralis in this study was relatively higher than that reported in study among pupils in Southwestern Cameroon [9], but comparable to that of another study on persons of all ages in the same Southeastern Cameroon [6]. Prevalence of infection could be higher but for the suboptimal sensitivities of the use of eggs/ova in sputum [10], compared to the good sensitivity and specificity of the ELISA method, especially ELISA using partially purified cysteine proteinases method [6, 11]. However, the repeated sputum examinations per person adopted in this study are known to improve the sensitivity of the parasitological method [1]. Another limitation in this study is that the parasitological method of egg/ova detection in sputum cannot detect those in the pre-patent period of infection or extra-pulmonary paragonimiasis [12].
The prevalence in this study was significantly higher in women. This is expected as a significantly higher proportion of crab eaters in the study area were females; only one-quarter were males. However, prevalence was comparable between both sexes in neighboring southwest area of Cameroon [9]. Many other researchers have reported no sex-related difference in prevalence [13, 14]. In contrast Singh and coworkers reported a higher prevalence among male patients in Manipur, India [15]. However, paragonimiasis is found in children, adults, and all categories of people [14]. On the whole, crab eating is common in Eastern Nigeria. It is quite popular and comparable in all the communities in the two major ethnocultural groups. However, the mean age of crab eaters is older (43 years) than that of noncrab eaters (26 years), indicating that crab eating is not as popular among the younger persons in Eastern Nigeria as among the older ones. This is encouraging as it would lower the risk of paragonimiasis infection over time.
Presently, the high popularity of crab eating explains the relatively high prevalence of paragonimiasis in Eastern Nigeria. More than a fifth of infected persons presented high intensities of egg/ova in sputum, while almost half of the infected persons presented low intensities. This in addition to the relatively high prevalence of infection buttresses the status of Eastern Nigeria as a paragonimiasis endemic area.
The higher the frequency of crab eating, the higher the risk of infection with paragonimiasis. Committed eaters such as weekly eaters had greater risk of being infected than monthly or yearly eaters. Surprisingly, the risk of infection was higher among irregular eaters than that of quarterly eaters. The reasons for this are not readily known. However, quarterly and yearly eaters could be regarded as curious or circumstantial eaters, while some of the irregular eaters could be incidental eaters who may eat more frequently at a time and less frequently at other times.
The frequency for some food-borne parasitic diseases is generally on the increase [16, 17]. Several of these may be directly linked to the dramatic increase in aquaculture, and they demonstrate how subtle changes in ecology, which may be economically driven, may contribute to an increased incidence of parasitic diseases [8].
Paragonimiasis is not popular among health policy makers in Southeastern Nigeria, probably because it causes very limited morbidity and with only occasional deaths. It has been called “benign endemic hemoptysis” [7]. Many patients are asymptomatic or have subclinical disease and are unaware of the infection, whereas others have mild-to-moderate symptoms for many years before they come to medical attention, if they ever come to medical attention at all [18]. Regardless of the mild nature of paragonimiasis in many patients, it remains an important cause of morbidity in many parts of the world [7] and therefore should come into focus in health policy thrusts in endemic areas. This has become necessary because of incessant loss of man hours as a consequence of the scourge in Southeastern Nigeria. Common complaints are associated with the scourge that result in loss of man hours include fever, chest pain, dyspnea, fatigue and urticaria, eosinophilia, diarrhea, gastroenteritis, in the early phases of the infection; and cough and recurrent hemoptysis in the chronic stage of the infection. Furthermore, the migrating worms may cause bronchiectasis, interstitial pneumonitis, transient hemorrhage, or bronchopneumonia to varying degrees [19, 20].
The implication of high prevalence of paragonimiasis in Southeastern Nigeria is its overlap with tuberculosis [21] and its consequent diagnostic confusion. The existence of another Paragonimus species, especially P. africanus, is most probable as southeastern is contiguous with Southwestern Cameroon, an area where the latter is predominant [6]. With a preponderance of unqualified personnel, and ill-equipped diagnostic laboratories, the problems of wrong diagnosis especially of tuberculosis would likely escalate. So many false positives would be subjected to the rigors of strong medications that could further complicate their health statuses by causing side effects and/or experiencing drug interactions [15, 22]. This informs the need to intensify awareness campaign in the epidemiology, clinical manifestations, and control of paragonimiasis in Southeastern Nigeria, especially on the dangers of eating improperly cooked crabs and crayfishes.
Substantially reduction in infections in countries that traditionally have had high incidences of infection has been directly related to educational efforts [3]. Therefore, mass education and awareness campaign to provoke changes in customs and food preparation practices should be emphasized in Southeastern Nigeria. The epidemiology and economic importance of paragonimiasis should be explained in such a way that majority of the people would be adequately informed about the risks of their food choices and food preparation preferences [7].
Conflict of Interests
The author declares that he has no conflict of interests.
Acknowledgments
The author thanks the health authorities of Bende, Okigwe, Oyigbo, Obio/Akpor, and Emohua Local Government Areas and the town heads of the respective communities that made up the study area for their assistance in creating awareness in their areas for the study.