Abstract: Background and Objective: Cockroaches pose significant public health problem due to their ability to mechanically transmit human intestinal parasites and other disease-causing micro-organisms. Hence this investigation was carried out to assess the prevalence and distribution of parasites associated with Periplaneta americana in Otefe-Oghara, Delta state, Nigeria. Materials and Methods: About 984 P. americana were collected from 4 sampling locations using jars baited with bread soaked in beer. The specimens were subjected to standard parasitological techniques for isolation of ecto and endo-parasites in each P. americana. Results: Of the 984 P. americana examined, 899 were infected with 13 parasites with an overall general prevalence of 79.89%. Of the 13 parasites encountered in this study, Ascaris lumbricoides had the highest prevalence (39.63%), closely followed by hookworm (35.77%). The prevalence of other parasites were in the following trend: Trichuris trichiura (32.72%), Strogyloides sterocalis (29.57), Giardia intestinalis (23.07), Entmoeba histolytica (19.00), Hymenolepsis nana (15.85), E. coli (13.11), Balantidium coli (12.91), Enterobius vermicularis (13.00), I. belli (8.13), Cryptosporidium parvum (2.95) and Taenia species (2.02). Two Factor ANOVA showed significant difference (p<0.05; F = 12.44; p = 1.9×10–09) in the prevalence of parasites and the studied locations (p<0.05; F = 24.80; p = 7.05×10–09). The exoskeletons of P. americana had more parasitic species that the alimentary tracts which was statistically significant (p<0.05; F = 4.61, p = 0.006). However, Pearson (r) correlation analysis showed a strong and positively significant value of 0.9378 between prevalence of parasites in the exoskeleton and alimentary canal. Conclusion: It is imperative to urgently institute control measures against P. americana through massive public enlightenment, education, improved sanitary conditions associated with proper waste management of landfills and fumigation of cockroach susceptible sites in Otefe-Oghara and its environ.
INTRODUCTION
Cockroaches (Hexapoda: Blattaria) are dorso-ventrally flattened, domestic, ubiquitous insects with an oval shape and a characteristic long moniliform antennae1. About 30 out of over 3,500 known cockroach species are associated with human habitation since antiquity1,2. Of these number, only 4 species (Periplaneta americana (Blattaria: Blattidae; Linnaeus, 1758), Blattella germanica, (Blattaria: Blattellidae; Linnaeus, 1767) and B. orientalis and Supella longipalpa) are considered as the most common notorious pest associated with households, supermarkets, public places and refuse dumps3,4. The P. americana commonly called American cockroach is a tropical and subtropical household pest particularly in Nigeria where they live in clusters. This species is of public health importance due to its association with human waste as well as its ability to traffic from sewers into homes and commercial establishments like restaurants. P. americana are attracted to dark and moist-warmth environment such as toilets, bathrooms, kitchens and basements.
Generally, cockroaches are known to be vectors of several diseases like dysentery, typhoid and polio as well as gastroenteritis. P. americana is a coprophagous vector, contaminating large quantity of consumable by leaving behind human faecal matter and parasitic cyst/eggs of helminths and protozoa. The P. americana does not only contaminate food with their faecal pellets, their filthy, breeding, habits, feeding mechanisms and indiscriminate travel between filth and food can also cause food poisoning5. The prevalence and morbidity of human parasitic infections in Nigeria, especially, in rural communities like Oghara are continuously high partly due to the vectorial role of P. americana6,7. Parasites of public health importance have been isolated from external surfaces and internal body parts of P. americana. Poor personal hygiene are epidemiological factors believed to encourage the spread of P. americana and sustenance of parasitic infections. Tropical parasitic infections like ascariasis, trichuriasis, amoebiasis, giardiasis, balantidiasis, taeniosis and Enterobius vermicularis are acquired either by ingestion of the eggs/cyst6 or by dermal penetration of skin by larva of Strongyloides stercoralis, hookworms, Schistosoma mansoni and S. haematobium8. Transmission is closely related to personal and environmental hygiene9. Epidemiological studies have documented these parasites to be vectored by P. americana3,4,10-12. The presence of P. americana in households is of epidemiological significance due to their nocturnal and filthy habits13, a characteristics feature that makes them an ideal carriers of pathogens.
Human population expansion has caused over 60% of cockroach populations to be isolated from urban areas, partly due to insufficient dumpsites, domestic waste accumulation, poor housing standards, over-crowding, inadequate water supplies and ignorance. The P. americana is the most abundant and obnoxious non-biting insect pests in Oghara metropolis, inhabiting residential buildings, hospitals, hostels, hotels, waste dumpsites and restaurants. Despite the abundance of P. americana in Oghara community, there is no documented data on their epidemiological and vectorial role in this study area. This research was carried out to: (1) Investigate the prevalence of parasites of public health importance in P. americana, (2) Establish the distribution and abundance of P. americana in four ecological niches and geographic locations and (3) Study the vectorial role of P. americana in the transmission of parasites eggs in Otefe-Oghara community, Delta state, Nigeria.
MATERIAL AND METHODS
Description of study area: This research was carried out between July and September, 2018, in Otefe-Oghara, a tropical academic community in Ethiope West Local Government Area, Delta state, Nigeria. The study area is located within the tropical rainforest belt in Nigeria on a geographical coordinate of Longitude 5°45'17'' N and Latitude 5°58'52'' E of the Greenwich meridian. The study area is an agglomeration of several communities aligned linearly along the River Jameson, Delta state. Physiographically, the area is a typical coastal plain terrain, monotonously lowland and flat with a gentle slope towards the Jameson River. Scarcity of good housing facilities elicited by the teeming population of Delta state Polytechnic students had resulted in overcrowded living conditions. The community lacks good environmental and personal hygiene services, with many piles of faecal matter in nearby residential areas. The proliferation of P. americana infestation can be attributed to pit latrine, multiple refuse dumpsite including the use of deformed, rusty, overflowed uncovered punctured bins and the untimely collection of refuse. The heavy flooding during the rainy season frequently increases sanitation problem. Inhabitants of the community are mainly farmers, few artisan, sand miners, students and civil servants. The study area was partitioned into 4 regions based on roads accessibility. A total of 80 houses (including hostels) were sampled from staff quarters (location 1: Latitude: 5°57'43'' N; Longitude: 5°45'17'' E), Mondele (location 2: Latitude: 5°58'52'' N; Longitude: 5°45'36'' E), Genesis (location 3: Latitude: 5°59'59'' N; Longitude: 5°45'44'' E) and Ibori quarters (location 4: Latitude: 5°59'1'' N; Longitude: 5°45'47'' E).
Cockroach collection and identification: Jars baited with bread soaked in beer were placed in kitchen, toilets/bathrooms, living and bedrooms in accordance with standard methods4,14. The inside portion of these jars were smeared with a thin film of petroleum jelly to prevent cockroach escape. The collection bottles were set at 18:00 h and collected by 07:00 h the next morning for 2 consecutive months. Collections of 1 cockroach per bottle were transported to Tropical Disease Research unit, Delta state University where they were anaesthetized and killed by chloroform fume for possible identification using standard entomological keys15,16. A total of 984 adult, whole P. americana, sorted by capture location were included in this study while those showing missing body parts were excluded.
Parasitological investigation
Please make the spacing visible in this highlighted text: Methods of Bala and Sule17 were employed in the isolation of ecto-parasites of cockroaches. Briefly, 2 mL of normal saline was added to the universal container with the cockroach and shaken vigorously for 2 min to detach the parasites on the surface of the cockroach and then filtered with a Cheese cloth. About 1 mL of the washing fluid was transferred to a centrifuge tube and centrifuged at 2000 rpm for 5 min. The supernatant was discarded and the deposits was placed on a clean glass slide, covered with a cover slip. Cysts and oocysts were identified by adding 1 drop of 1% Lugol’s iodine at the border of the cover slides and the preparation was observed at 40x microscope objective lens for the identification of parasites.
Isolation of parasites from gastrointestinal tract of cockroaches: Washed P. americana were individually placed and rinsed in a flask containing 70% ethanol for 5 min. They were transferred to another sterile flask to air dry at room temperature (25°C) and then washed with normal saline for 3 min to remove the alcohol. After washing, each P. americana were fixed on a dissecting petri dish where the head and appendages were severed and the abdomen was opened using fine pointed forceps with small scissors. The gut and other abdominal organs were lifted with a teasing needle and a small forceps and washed in a vial containing 5 mL of saline solution. The gastrointestinal tract were finely macerated into tiny bits by means of sterile scalpel blade then filtered with a Cheese cloth. About 2 mL of the filtrate was centrifuged at 2000 rpm for 5 min and the deposits placed on a clean glass slide, stained with 1% Lugol’s iodine. Each slides was stained with modified acid fast stain and Ziehl-Neelsen staining method for Isospora belli, Endolimax nana and Cryptosporidium oocysts, respectively18. The slides were examined microscopically for ova, oocyst, larva and cysts of parasites present at X10 and X40 objective lens and identified using standard taxonomical keys19,20. Specimens which could not be processed immediately were kept in the refrigerator2,17 at -4°C.
Data analysis: Data were analyzed using descriptive statistics, percentage and frequencies; cross tabulation of the outcome was performed. One-way analysis of variance (ANOVA) test was used to determine the association and significant difference between the distribution of cockroaches and the parasites identified. Subsequently, t-test analysis was used to determine association and significant differences between the parameters tested. All results were considered significant at the 95% confidence interval and significance level was set at p<0.05.
RESULTS
Prevalence of parasites based on gender and ecological niche: Of the 984 P. americana examined, 899 were infected with 13 parasites with an overall general prevalence of 91.36%. About 587 males (59.65%) were infected, while the females had 31.71% prevalence of the 363 P. americana examined. The prevalence of parasites in P. americana captured from toilet was higher (99.19%) than kitchen, bedroom and living room with respective values of 95.39, 83.15 and 56.79% in the study area (Table 1).
Based on the general P. americana population, Fig. 1 indicated the eco-niche prevalence of parasites. Irrespective of eco-niche, 8.64% of P. americana were uninfected with parasites. The least eco-niche prevalence was recorded in P. americana obtained from living rooms (Fig. 1).
| Table 1: | Prevalence of P. americana parasites within households in the study area |
| N.I: No. infected | |
| Table 2: | Prevalence of parasites associated with P. americana in four selected locations in Otefe-oghara, community |
| Data presented in parenthesis are prevalence values of each parasite isolated, S.E: Standard Error | |
| Fig. 1: | Eco-niche prevalence of parasites vectored by P. americaca |
Prevalence of specific parasites and geographical location: Out of the 13 parasites encountered in this study, A. lumbricoides had the highest prevalence (39.63%), closely followed by hookworm (35.77%). The prevalence of other parasite in this study were in the following trend: T. trichiura (32.72%), S. sterocalis (29.57), G. intestinalis (23.07), E. histolytica (19.00), H. nana (15.85), E. coli (13.11), B. coli (12.91), E. vermicularis (13.00), I. belli (8.13), C. parvum (2.95) and Taenia species (2.02) (Table 2). Further evaluation revealed that A. lumbricoides had 59.51% as the prevalence value. All parasites encountered in this study were present in location 2, 3 and 4 except for location 1 which had no prevalence for C. parvum (Table 2). Taenia species had the least prevalence of parasitic infection in all locations. Results shown in Table 2 indicated that, P. americana in location 1 were least infected. In this investigation, location 4 (Ibori quarters) had the highest prevalence (94.33%) of parasitic infection (Table 2). This was followed by location 2 (Mondele) with a prevalence of 82.43%. Next on the prevalence scale was location 3 (Genesis quarters) with a value of 77.11%. While the least prevalence was recorded in location 1 (staff quarters) with a value of 64.02%. Statistically, two factor analysis of variance (ANOVA) showed significant difference (p<0.05; F = 12.44; df = 12; p = 1.9×10–09) in the prevalence of parasites encountered and the studied locations (p<0.05; F = 24.80; df = 3; p = 7.05×10–09). However, t-test indicated that there was no significant difference (p>0.05) in the prevalence between location 1 vs. 2; 1 vs. 3; 1 vs. 4; 2 vs. 3; 2 vs. 4 since tStatistics (-3.6742, -5.6581, -4.1985, -5.9003, -1.1344, respectively) <tcritical two tail (2.1788) except location 3 vs. 4 (tstat = 5.1556) which was statistically significant at 0.05 level of significance.
Prevalence of parasites eggs/cysts in exoskeleton and digestive tracts based on location: This study further indicate that high number parasitic eggs/cyst were encountered in the external surface (exoskeleton) of P. americana than was found in the alimentary tract (Table 3, 4). Statistically, there was significant difference (p<0.05) in the mean prevalence of parasitic species isolated from the exoskeleton and alimentary canal (internal organs) of P. americana (Parasitic species: F = 4.61, p = 0.006, df = 12 and site of isolation (external/internal): F = 54.47, p = 8.5×10–06, df = 12).
| Table 3: | Mean prevalence of parasites from exoskeleton and alimentary tract of Periplaneta americana in the study area |
| Table 4: | Prevalence of parasites associated with P. americana in four selected locations in Otefe-oghara, community |
| N.I: Number of infected, Data presented in parentheses are prevalence values of each parasite isolated | |
However, Pearson (r) correlation analysis showed a strong and positively high value of 0.9378 (93.78%) between prevalence of parasites in the exoskeleton and alimentary canal of P. americana. Furthermore, t-test analysis revealed significant difference (p>0.05) in the prevalence between parasites associated with external surfaces and alimentary tract since tstatistics (7.3802) >tcritical two tail (2.1788) at 0.05 level of significance.
DISCUSSION
There is a dearth of epidemiological reports on the vectorial role of P. americana in the transmission of human parasitic diseases in Delta State, Nigeria. This present study had incriminated P. americana as a mechanical vectors of intestinal parasitic infections in Oghara community. Preliminary reports in Africa3,13,21 particularly in Nigeria2,4,10,12,22 had documented P. americana as a paratenic vector of several human intestinal parasites. The current study showed that all the parasites isolated from P. americana are of medical importance and have been implicated in many gastrointestinal disorder. This study further indicated that the prevalence of parasites in the external surfaces of P. americana is higher compared to the internal tracts. This was substantiated by Etim et al.2 who documented 65.3% for external surfaces and 34.6% for internal organs. Similarly, high (72.5 and 88.5%) parasitic infection were observed on the external surfaces of cockroaches caught from the hospital environment and residential areas, respectively21.
It is evident in this present study that the overall parasites recovered from the external surface were more than those recovered from gut of P. americana. This marginal disparity could be explained in 2 ways, it could be that the P. americana only have body contacts with the parasites without ingesting them or the parasites were unable to survive in the cockroaches studied. Both reasons are valid given the fact that some of the ova/cysts of the parasites encountered in this study are sensitive to changes in environmental factors23,24.
A wide range of parasitic composition were isolated from the P. americana sampled, a rare observation by other studies10,11,25. This study recovered 13 parasites belonging to 2 taxonomic groups: Helminths (hookworm, A. lumbricoides, T trichiuria, Taenia spp., E. vermicularis, S. stercoralis) and Protozoan (E. histolytica, E. coli, H. nana, G. intestinalis, B. coli, C. parvum, I. belli) parasites of medical importance similar to earlier reports26. The number of protozoan parasites were more in number but not in occurrence compared to the helminths group. The prevalence (39.63%) of A. lumbricoides obtained in this study is higher than 27.40, 13.20 and 33.60%, respectively recorded by other researchers2,10,25. Contrarily, Oyeyemi et al.22 recorded a higher prevalence of 52.30%.
The most prevalent parasites encountered in this study were hookworm and A. lumbricides and T. triciura corroborated by earlier reports14. Findings from Osogbo, Oyo state, Nigeria27 and Ghana28 also reported hookworm (49%) as the most frequently common parasite of P. americana. The high occurrence of A. lumbricoides and hookworm, not only on the cockroaches but in the environment and faecal sample over other gastrointestinal parasites has also been documented in human populations in Africa, West Africa, Nigeria6,29. The risk of transmissions has been associated with poor sanitary condition30. Other species of the helminths order also formed a larger part of the overall total of parasites identified and isolated in this result. The T. tirchiuria, S. stercorahs and E. vermicalaris were identified from previous report in Ethopia26. The occurrence of E. histolytica observed in their study, might probably be because of the resistance conferred by the cyst wall, which makes the cysts to survive days to weeks in the external environment and probably be vectored by cockroaches and other synanthropic insects.
The vectorial potential of cockroaches have also been reported17. They documented E. vermicularis which indicates that the cockroaches had contact with infected patients or contaminated clothes which emphasizes their vectorial potential for parasitic diseases. The occurrence of E. histolytica might be because of resistance conferred by the cysts wall, which make the cysts to survive days to weeks in the external environment and probably be vectored by cockroaches and other synanthropic insects.
CONCLUSION AND RECOMMENDATIONS
The findings of this study shows that P. americana in the study area are potential vectors of parasitic disease. The parasites eggs, cyst, oocyte encountered in this study are of medical importance. It is imperative to urgently institute control measures on these insects through massive public health/enlightenment education on improving the existing standard of environmental sanitary conditions such as general cleanliness, proper discarding of leftover food, timely washing of dishes and rinsing of cans or bottles before disposal and the use of cockroach-proof garbage bins should be instituted at home. Periodic fumigation and proper management of landfills are also recommended in the control of this insect pest (cockroach).
SIGNIFICANCE STATEMENT
This study revealed that P. americana is an important epidemiological factor in the transmission of several tropical parasites. This study identified 13 parasites isolated in P. americana from four ecological niches. P. americana captured from toilets had the highest (99.19%) prevalence of parasites, followed by kitchen, bedroom and living room with respective values of 95.39, 83.15 and 56.79%. This study further indicate that high number parasitic eggs/cyst were encountered in the external surface of P. americana than the alimentary tract. The parasites isolated from P. americana causes human diseases of public health importance. The prevalence of these parasites are detrimental to human capital development, because they affect work efficiency and outputs. This study will help parasitologist, entomologist, the general public, governmental and non-governmental organisations in proper management of vectors and diseases associated with P. americna.
ACKNOWLEDGMENT
Research assistance received from Center for Research in Environmental Resource Management (CREMA) and Tropical Disease Research (TDR) Unit, Delta State University, Nigeria is highly appreciated.