Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T12:42:33.890Z Has data issue: false hasContentIssue false

Influence of tides on the dissemination and related health risks of intestinal helminths along the Kribi beaches (Atlantic Coast, Southern Cameroon)

Published online by Cambridge University Press:  24 January 2024

P.A. Nana*
Affiliation:
Department of Oceanography, Institute of Fisheries and Aquatic Sciences, University of Douala, P.O. Box 7236, Douala, Cameroon
S. Tchakonté
Affiliation:
Laboratory of Natural Resources and Environmental Management, Faculty of Science, University of Buea, P.O. Box 063, Buea, Cameroon
M. Pahane Mbiada
Affiliation:
Department of Processing and Quality Control of Aquatic Products, Institute of Fisheries and Aquatic Sciences, University of Douala, P.O. Box 7236, Douala, Cameroon
A.L. Fotseu Kouam
Affiliation:
Laboratory of Hydrobiology and Environment, Faculty of Science, University of Yaoundé 1, P.O. Box 812, Yaoundé, Cameroon
R.S. Mouchili Palena
Affiliation:
Department of Oceanography, Institute of Fisheries and Aquatic Sciences, University of Douala, P.O. Box 7236, Douala, Cameroon
G. Bricheux
Affiliation:
Laboratoire Microorganismes: Génome et Environnement (LMGE), UMR CNRS 6023, Université Clermont Auvergne, 63178 Aubière, France
M. Nola
Affiliation:
Laboratory of Hydrobiology and Environment, Faculty of Science, University of Yaoundé 1, P.O. Box 812, Yaoundé, Cameroon
T. Sime-Ngando
Affiliation:
Laboratoire Microorganismes: Génome et Environnement (LMGE), UMR CNRS 6023, Université Clermont Auvergne, 63178 Aubière, France Laboratoire Magmas et Volcans (LMV), UMR CNRS 6524, UMR IRD 163, Université Clermont Auvergne, 63178 Aubière, France
*
Corresponding author: P.A. Nana; Email: nanapaul4life@yahoo.fr
Rights & Permissions [Opens in a new window]

Abstract

Kribi is a seaside town that welcomes thousands of tourists each year. However, the poor sanitation condition of its beaches along the Atlantic coast is not without risk for visitors. In this study, we used the formol-ether concentration technique to identify and quantify larvae or eggs of intestinal helminths in waters of three regularly visited Kribi beaches (Mpalla, Ngoyè, and Mboamanga). Results revealed that all identified larvae and eggs were cestodes (Hymenolepis nana) and nematodes (Strongyloides sp., Ascaris sp., Ancylostoma duodenale and Trichuris trichiura). All the helminth eggs and larvae showed high abundance at low tide during rainy seasons. Ancylostoma duodenale eggs, totally absent at Mpalla, were densely present at low tide at Ngoyè (301 ± 15 eggs/L). Trichuris trichiura eggs showed the lowest abundance (0 to 62 eggs/L) at all sites. Abiotic variables indicated that waters at the various beaches were basic (pH: 8.75–9.77), generally warmer (32.44°C at Mpalla in the Short Rainy Season), more oxygenated at low tide, and moderately mineralized at high tide. Positive and significant correlations were observed at Ngoyè at low tide between Strongyloides sp. larvae and dissolved oxygen (P ˂ 0.05); and between Ancylostoma duodenale eggs and temperature (P ˂ 0.05). The overall results indicated that the beaches studied are subjected to fecal pollution. This pollution is more accentuated during low tides than during high tides. Depending on tidal movements, swimmers risk exposure to helminth eggs and larvae known to be responsible for gastroenteritis.

Type
Research Paper
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Introduction

Microbiological pollution represents one of the major problems to which coastal and marine environments are subjected (Dang & Lovell Reference Dang and Lovell2016; Basili et al. 2021; Oduro et al. 2023). It refers to the presence of microbial organisms in these ecosystems, such as bacteria, viruses, or parasites, some of which may be pathogenic to humans or animals (Nimnoi & Pongsilp Reference Nimnoi and Pongsilp2020). Although marine and coastal ecosystems are the natural environment for some microorganisms, those involved in microbiological contamination of coastal waters are of human or animal origin (Rodríguez et al. 2021; Manini et al. 2022). These are enteric microorganisms, i.e., from the intestines of humans or warm-blooded animals and brought into the environment via their excreta. Sources of this excreta include discharges of treated and untreated sewage on land and from ships’ ballast water, livestock effluents (animal faeces), stormwater discharges, rainfall-runoff, and other diffuse sources (Assako Assako et al. Reference Assako Assako, Tonmeu Djilo, Bley, Vernazza-Licht, Gruénais and Bley2010; Manini et al. Reference Manini, Baldrighi, Ricci, Grilli, Giovannelli, Intoccia, Casabianca, Capellacci, Marinchel, Penna, Moro, Campanelli, Cordone, Correggia, Bastoni, Bolognini, Marini and Penna2022).

The concentration and dissemination rate of these organisms depends on tidal range, rainfall, turbidity, and hydrodynamics, among other factors (Di Biase & Hanssen Reference Di Biase and Hanssen2021). Tides, approximately two highs and two lows per day, generate and influence ocean currents (Madani et al. Reference Madani, Seth, Leon, Valipour and McCrimmon2020). In turn, these currents directly and indirectly affect the movement of aquatic fauna (seedlings, fish) and the dispersion of microbes. Like the tide, winds, underwater topography, and weather conditions influence the dispersal of microorganisms (Ferrarin et al. Reference Ferrarin, Penna, Penna, Spada, Ricci, Bilić, Krzelj, Ordulj, Šikoronja, Đuračić, Iagnemma, Bućan, Baldrighi, Grilli, Moro, Casabianca, Bolognini and Marini2021; Kraus et al. Reference Kraus, Baljak, Vukić Lušić, Kranjčević, Cenov, Glad, Kauzlarić, Lušić, Grbčić, Alvir, Pećarević and Jozić2022).

Bacteria and viruses introduced into the marine environment can affect bathing water quality and cause health impacts, which can lead to the closure of the affected areas if the contamination is significant and persistent (Bonadonna et al. Reference Bonadonna, Briancesco, Suffredini, Coccia, Della Libera, Carducci, Verani, Federigi, Iaconelli, Bonanno Ferraro, Mancini, Veneri, Ferretti, Lucentini, Gramaccioni and La Rosa2019; Manezeu Tonleu et al. Reference Manezeu Tonleu, Nana, Onana, Nyamsi Tchatcho, Tchakonté, Nola, Sime-Ngando and Ajeagah Aghaindum2021). Helminthiasis is one of the most common infections in the world, disproportionately impacting the poorest and most disadvantaged communities (WHO 2006). They are transmitted by eggs in human excreta, which then contaminate soil where sanitation conditions are inadequate (Collender et al. Reference Collender, Kirby, Addiss, Freeman and Remais2015; Truscott et al. Reference Truscott, Turner, Farrell and Anderson2016; Walusimbi et al. Reference Walusimbi, Lawson, Nassuuna, Kateete, Webb, Grencis and Elliott2023). Bathing in water of poor microbiological quality thus presents health risks and can lead to infections, mainly gastroenteritis caused by helminth eggs or larvae (WHO 2006; Bonadonna et al. Reference Bonadonna, Briancesco, Suffredini, Coccia, Della Libera, Carducci, Verani, Federigi, Iaconelli, Bonanno Ferraro, Mancini, Veneri, Ferretti, Lucentini, Gramaccioni and La Rosa2019; Manezeu Tonleu et al. Reference Manezeu Tonleu, Nana, Onana, Nyamsi Tchatcho, Tchakonté, Nola, Sime-Ngando and Ajeagah Aghaindum2021). In rare cases, contaminated water can also lead to more serious infectious diseases such as typhoid fever, cholera, etc. (WHO 2019).

In sub-Saharan Africa in general and in Cameroon in particular, microbiological data and standards on beach water are rare and almost non-existent, yet these environments constitute high contamination sites due to their high frequency of use year-round. This poses an ecological and public health problem on Cameroonian beaches in general and those of Kribi in particular. This study investigates the influence of tidal cycles on the diversity and abundance of intestinal helminth larvae and eggs in the waters of Kribi beaches. We hypothesized that dispersion of intestinal helminths would be influenced by the tidal cycle. To evaluate the impact of the tidal cycle on the dissemination of intestinal helminths in the waters of the city of Kribi, Southern Cameroon Region, we qualitatively and quantitatively compared pathogen concentrations at high and low tide on three Kribi beaches (Mpalla, Ngoyè, and Mboamanga).

Materials and methods

Study area

The study was conducted from April to December 2021 on the three most frequented beaches of the city of Kribi, in the Ocean Division, southern Atlantic coast, Cameroon (Figure 1). This area is subject to a Guinean-type equatorial climate, characterized by four seasons: Long Dry Season (LDS) from December to February, Short Rainy Season (SRS) from March to May, Short Dry Season (SDS) from June to July, and Long Rainy Season (LRS) from August to November (Olivry Reference Olivry1986). Four sampling campaigns were conducted: April (SRS), July (SDS), September (LRS), and December (LDS), respectively. At the level of each beach, one sampling station was surveyed based on its accessibility and frequentation. Station 1 is located at Mpalla beach (3◦00’29”N–0009◦56’54.5”E) and characterized by a gray sandy substrate. Station 2 is situated at Ngoyè (2◦57’26.6”N–0009◦54’36.9”E), 4 km from Mpalla, and characterized by a black sandy substrate. Located 9 km from Ngoyè, station 3 on Mboamanga beach (02◦56’22.4”N–0009◦54’12.3”) is characterized by a sandy clay gray substrate.

Figure 1. Location map showing sampling points.

Measurement of hydrodynamic and abiotic parameters

At each tidal cycle, water depth was recorded using a Plastimo ECHOTEST II (Lorient Cedex - France) handheld depth sounder. Current velocity was assessed by float gauging using a limnimetric scale, float, chronometer, and decameter (Ngoma & Wang Reference Ngoma and Wang2018).

Physicochemical parameters were analyzed according to Rodier et al. (Reference Rodier, Legube and Merlet2009) and APHA (2017) standard methods. At each campaign and each sampling station, eight physico-chemical parameters were measured in situ, in triplicate during each tide period (low and high tide), using a hand-held multiparameter (HANNA/HI98494Tanneries Cedex - France). These variables included pH, temperature (°C), salinity (PSU), dissolved oxygen content (mg/L), total dissolved solids (g/L), electrical conductivity (mS/cm), resistivity (Ω/cm), and pressure (mbar).

Collection and treatment of biological samples

At each station, for each season, water samples were collected at high and low tide in 1000 mL sterile polyethylene bottles. In the laboratory, for the identification and enumeration of helminths, the samples were first left for 24 h at room temperature in the sedimentation flasks. After sedimentation, the supernatant was decanted and the muddy deposit obtained was then measured, homogenized, and distributed in test tubes. The formol-ether concentration technique enabled us to concentrate the helminth eggs or larvae to guarantee better enumeration (Suwansaksri et al. Reference Suwansaksri, Nithiuthai, Wiwanitkit, Soogarun and Palatho2002; Collender et al. Reference Collender, Kirby, Addiss, Freeman and Remais2015). Therefore, in each test tube, 1 mL of 10% formalin, 5 mL of distilled water, and 2–3 drops of Lugol were added. The tubes were then centrifuged at 500 rpm for 5 min using a centrifuge (Medifriger, Barcelona - Spain). Each time, the entire pellet was recovered and placed on slides for direct observation and enumeration of eggs or larvae under an optical microscope (Olympus Model CK2, Hamburg - Germany) (Ajeagah & Fotzeu Kouam Reference Ajeagah and Fotseu Kouam2019). The helminth eggs or larvae were identified using the WHO manual (2019) and the Thivierge workbook (Reference Thivierge2014). The number of eggs or larvae contained in 1 L of sample was obtained by the following formula, proposed by Ajeagah et al. (Reference Ajeagah, Foto Menbohan, Talom, Ntwong, Tombi, Nola and Njine2014):

$$ \boldsymbol{X}=\frac{\boldsymbol{y.Vx}}{\boldsymbol{Vy}} $$

$ \boldsymbol{X} $ = number of parasites, $ \boldsymbol{Vx} $ = volume of the pellet of 1 L of sample, $ \boldsymbol{Vy} $ = volume of the pellet used for observation, $ \boldsymbol{y} $ = number of parasites observed in $ \boldsymbol{Vy} $

Data analysis

As the sample concentrations had a normal distribution, the linear correlation coefficient r (Pearson) was used to calculate the dependency between the quantitative variables (biotic and abiotic). SPSS software version 16.0 allowed us to perform correlation tests. P values were used to assess the significance of the correlation between abiotic and biotic parameters. The safety threshold was 5% (P ˂ 0.05).

Results

Hydrodynamic and abiotic variables

At the different sites surveyed, the average water depth varied between 0.42–0.83 m at low tide and 1.81–2.10 m at high tide (Table 1). Concerning current velocity values were globally higher at low tide than at high tide. The lowest average current velocity (0.89 m/s) was recorded at high tide, at Ngoyè.

Table 1. Some hydrodynamic characteristics of the surveyed sites

Min.: minimum; Max.: maximum; x̄: average; σ: standard deviation; N=8 (for each sampling site)

Abiotic parameters varied according to two aspects: time and tidal cycles (Figure 2). At both high and low tide, waters were strongly basic at all beaches across the study period. The highest pH value (9.77) was recorded at Mboamanga in SRS, whereas the lowest (8.75) was recorded in LDS at Mpalla, during high tide (Figure 2A). At high tide, the water temperature varied from 28.16°C in LDS at Ngoyè to 31.75°C in SRS at Mboamanga. At low tide, temperature ranged from 29.34°C in LDS at Mboamanga to 32.44°C in SRS at Mpalla (Figure 2B). At all stations, the warmest waters were recorded at low tide. Spatial and temporal variation of salinity did not differ significantly for any tidal cycle. The minimum salinity (30.87 PSU) was recorded in SRS, at low tide at Ngoyè, and the maximum value (36.19 PSU) in SDS, at high tide at Mboamanga (Figure 2C). The waters of Mpalla and Ngoyè beaches were poorly oxygenated at high tide compared to low tide throughout the study. Maximum values (0.70 mg/L) of dissolved oxygen were recorded in SRS, at high and low tides (Figure 2D). Total dissolved solids changed from 26.39 to 27.45 g/L at high tide and from 24.24 to 27.25 g/L at low tide (Figure 2E).

Figure 2. Physicochemical variables according to seasons and tidal cycles. SRS: Short Rainy Season; SDS: Short Dry Season; LRS: Long Rainy Season; LDS: Long Dry Season.

With values of electrical conductivity ranging from 48.28 μS/cm in LDS to 47.88 μS/cm in LRS at low tide, Ngoyè appeared to be the less mineralized beach (Figure 2F). Concerning resistivity, values were higher at Ngoyè than at other stations, and the maximum value (21 Ω/cm) was recorded at low tide in SRS (Figure 2G). Thus, the more mineralized the waters of the studied beaches were, the more concentrated the ions were, and, consequently, the higher electrical conductivity was. At the same time, the resistivity of these waters was low. Overall, the pressure was slightly lower at high tide than at low tide. Nevertheless, the lowest value (1015.73 mbar) was recorded at high tide in Mpalla in SDS (Figure 2H).

Diversity, distribution, and abundance of helminths

In this study, five species of intestinal helminths were identified in the waters of Kribi beaches. They belong to the Cestode class (Hymenolepis nana) and Nematode phylum (Strongyloides sp., Ascaris sp., Ancylostoma duodenale and Trichuris trichiura). Their abundances varied from one station to another and especially with tidal cycles (Table 2).

Table 2. Helminth eggs or larvae abundance recorded in the different sites

Min.: minimum; Max.: maximum; x̄: average; σ: standard deviation; N=8 (for each sampling site)

The eggs of H. nana were identified at all sites during low tide, while at high tide they were scarce. Maximum concentrations were recorded in LDS at low tide (18 eggs/L) and in SDS at high tide (35 eggs/L) at Ngoyè (Figure 3A). Mboamanga beach was the least contaminated with H. nana. Larvae of Strongyloides sp. were identified at all the sites sampled. On the beaches of Mpalla, Ngoyè, and Mboamanga, we counted, on average, 15, 34, and 13 Strongyloides sp. larvae per liter of water at high tide versus 21, 44, and 26 larvae/L at low tide, respectively. Regardless of the tidal cycle, the waters of Ngoyè had a high concentration of Strongyloides sp. larvae in contrast to the other beaches (Figure 3B). Across the study period, the abundance of Ascaris sp. eggs was three times higher at low tide than at high tide (Figure 3C). Across all sites, an average of 17 eggs/L was noted at high tide, against 50 eggs/L counted at low tide. During the study period and regardless of the tidal cycle, no A. duodenale eggs were identified in Mpalla (Figure 3D). Ngoyè beaches were the most contaminated, with an average of 18 eggs/L counted at low tide and 75 eggs/L at high tide. Unlike the other intestinal helminths, T. trichiura showed very low abundance at all the sites surveyed (Figure 3E). At Mpalla beach, a mean value of 3 eggs/L was recorded at high tide against 16 eggs/L at low tide. At Mboamanga, T. trichiura eggs were only identified in LDS at low tide (3 eggs/L).

Figure 3. Helminth eggs or larvae abundanceaccording to seasons and tidal cycles. (A) Hymenolepis nana; (B) Strongyloides sp.; (C) Ascaris sp.; (D) Ancylostoma duodenale; (E) Trichuris trichiura. SRS: Short Rainy Season; SDS: Short Dry Season; LRS: Long Rainy Season; LDS: Long Dry Season.

Correlation between physicochemical and biological variables

At all the beaches surveyed, significant correlations were revealed between certain physicochemical and microbiological parameters. At Mpalla, a positive and significant correlation was observed, at low tide, between concentration of T. trichiura eggs and total dissolved solids (r = 0.821, P = 0.047). At Ngoyè, positive and significant correlations were observed, at low tide, between concentrations of Strongyloides sp. larvae and dissolved oxygen (r = 0.781, P = 0.039, and r = 0.728, P = 0.042); and between concentrations of A. duodenale eggs and temperature (r = 0.836, P = 0.041, and r = 0.735, P = 0.036). At Mboamanga, at low tide, concentrations of Strongyloides sp. and Ascaris sp. were positively correlated with temperature (r = 0.738, p = 0.040, and r = 0.733, P = 0.039). In contrast, at high tide, concentration of T. trichiura eggs was negatively correlated with pH (r = -0.738, P = 0.041).

Discussion

In Kribi, rivers and beaches are used extensively by the populations (Batanga, Ngoumba, Mabéa, etc.) for bathing, washing dishes, laundry, fishing, and even for traditional ceremonies (Assako Assako et al. Reference Assako Assako, Tonmeu Djilo, Bley, Vernazza-Licht, Gruénais and Bley2010). However, poor management of these aquatic ecosystems can make the water resource dangerous, exposing populations to health risks (Nana et al. Reference Nana, Pahane Mbiada, Tchakonté, Moche, Mouchili Palena, Nola and Sime-Ngando2023a).

Globally, helminthiasis is one of the most common infections in the world, disproportionately impacting the poorest and most disadvantaged communities (WHO 2019). These infrections are transmitted by eggs in human excreta, which contaminate soil and water where sanitation conditions are inadequate (Schiefke et al. Reference Schiefke, Schmäschke, Ott, Schiefke, Mössner and Schubert2006; Walusimbi et al. Reference Walusimbi, Lawson, Nassuuna, Kateete, Webb, Grencis and Elliott2023). All the helminth species identified in this study are potentially responsible for human disease. H. nana is a cestode responsible for hymenolepiasis. It manifests itself through abdominal pain, nausea, slight emaciation, and anemia in case of massive infestation (Ikumapayi et al. Reference Ikumapayi, Sanyang and Pereira2019; Coello Peralta et al. Reference Coello Peralta, Salazar Mazamba, Pazmiño Gómez, Cushicóndor Collaguazo, Gómez Landires and Ramallo2023). Strongyloides sp. is a nematode responsible for Strongyloidosis or anguillulosis or “cutaneous larva migrans”. It causes skin lesions at the point of larval entry, possible inflammatory pulmonary reaction with dry cough during larval migration, enteritis with abdominal pain, and diarrhoea (Schär et al. Reference Schär, Trostdorf, Giardina, Khieu, Muth, Marti, Vounatsou and Odermatt2013; Lupia et al. Reference Lupia, Crisà, Gaviraghi, Rizzello, Di Vincenzo, Carnevale-Schianca, Caravelli, Fizzotti, Tolomeo, Vitolo, De Benedetto, Shbaklo, Cerutti, Fenu, Gregorc, Corcione, Ghisetti and De Rosa2023). Ascaris sp. is a nematode, responsible for ascariasis. At the beginning, the disease is manifested by respiratory disorders with fever at 38°C, dry cough, sometimes productive coughing, and breathing difficulties. Later on, digestive disorders, nausea, vomiting, abdominal pain, loss of appetite, and diarrhoea can emerge (Silver et al. Reference Silver, Kaliappan, Samuel, Venugopal, Kang, Sarkar and Ajjampur2018; Holland et al. Reference Holland, Sepidarkish, Deslyper, Abdollahi, Valizadeh, Mollalo, Mahjour, Ghodsian, Ardekani, Behniafar, Gasser and Rostami2022). A. duodenale is a nematode, responsible for hookworm disease or Ankylostomiasis. It manifests itself through itchy skin, followed by a skin rash on the feet and hands, and then bronchitis with coughing fits. It later evolves towards the chronic form with notable digestive and nervous disorders and anemia (Kucik et al. Reference Kucik, Martin and Sortor2004; Walusimbi et al. Reference Walusimbi, Lawson, Nassuuna, Kateete, Webb, Grencis and Elliott2023). T. trichiura is a nematode responsible for trichuriasis. It is more often benign or asymptomatic. If the parasite is abundant, colic (abdominal pain, diarrhoea) can be complicated by rectal hemorrhaging (Badri et al. Reference Badri, Olfatifar, Wandra, Budke, Mahmoudi, Abdoli, Hajialilo, Pestehchian, Ghaffarifar, Foroutan, Hashemipour, Sotoodeh, Samimi and Eslahi2022; Guilavogui et al. Reference Guilavogui, Verdun, Koïvogui, Viscogliosi and Certad2023). These species have been identified on Kribi beaches where tidal conditions had an impact on the quality and abundance of the helminth larvae or eggs. Contamination is favored at low tides by low flows, due to less dilution of water (Madani et al. Reference Madani, Seth, Leon, Valipour and McCrimmon2020). At the shoreline level, periods of spring tides, due to high tidal coefficients, would be the most favorable for the dilution of pollution (Kraus et al. Reference Kraus, Baljak, Vukić Lušić, Kranjčević, Cenov, Glad, Kauzlarić, Lušić, Grbčić, Alvir, Pećarević and Jozić2022; Nana et al. Reference Nana, Ebonji Seth, Ndjuissi Tamko, Onambélé Ossomba, Bricheux, Metsopkeng, Nola and Sime-Ngando2023b). These conditions would favor high concentrations of parasites in the water at low tide. Whether in Mpalla, Ngoyè, or Mboamanga, the highest concentrations of Strongyloides sp. larvae and Ascaris sp. eggs are linked to the great capacity of these parasites to adapt to variations in environmental conditions (Fotseu Kouam & Ajeagah Reference Fotseu Kouam and Ajeagah2019; Manezeu Tonleu et al. Reference Manezeu Tonleu, Nana, Onana, Nyamsi Tchatcho, Tchakonté, Nola, Sime-Ngando and Ajeagah Aghaindum2021). In contrast, the low abundance of T. trichiura eggs in all the sampled sites could be related to the high salinity of the waters.

It is possible to identify several causes of contamination that can explain the arrival of these faecal microorganisms on the Kribi beaches in lower vs. higher quantities. The contamination from human beings is mainly related to a total absence of wastewater treatment systems in this seaside town. Indeed, the city of Kribi, which has experienced a demographic boom in recent years, has no real wastewater and sewage sludge treatment system (Assako Assako et al. Reference Assako Assako, Tonmeu Djilo, Bley, Vernazza-Licht, Gruénais and Bley2010). Wastewater treatment plants are non-existent. Naturally, any absence or defect in the collective sanitation system can lead to the discharge of untreated water into the aquatic environment, resulting in the introduction of potentially pathogenic micro-organisms into the natural environment (Basili et al. Reference Basili, Campanelli, Frapiccini, Marco Lunaa and Queroa2021; Rodríguez et al. Reference Rodríguez, Gallampois, Haglund, Timonen and Rowe2021; Oduro et al. Reference Oduro, Darko, Blankson and Mensah2023). Non-sewage facilities can also generate contamination if they do not comply and discharge untreated effluent into the natural environment (Mohammed et al. Reference Mohammed, Echeverry, Stinson, Green, Bonilla, Hartz, McCorquodale, Rogerson and Esiobu2012; Soto-Varela et al. Reference Soto-Varela, Rosado-Porto, Bolívar-Anillo, Pichón González, Granados Pantoja, Estrada Alvarado and Anfuso2021). Other activities practiced on the Kribian coast could lead to the input of helminths from humans into the environment, particularly recreational activities, especially when boats are inhabited and do not have a sewage recovery system. Faecal pollution due to these activities is mainly located in marinas and fishermen’s camps. Contamination linked to recreational activities (swimming, restaurants) remains secondary (Weiskerger et al. Reference Weiskerger, Brandão, Ahmed, Aslan, Avolio, Badgley, Boehm, Edge, Fleisher, Heaney, Jordao, Kinzelman, Klaus, Kleinheinz, Meriläinen, Nshimyimana, Phanikumar, Piggot, Pitkänen, Robinson, Sadowsky, Staley, Staley, Symonds, Vogel, Yamahara, Whitman, Solo-Gabriele and Harwood2019; WHO 2021).

Rainfall would thus constitute one of the main vectors for the dissemination of helminth eggs or larvae (Manz et al. Reference Manz, Clowes, Kroidl, Kowuor, Geldmacher, Ntinginya, Maboko, Hoelscher and Saathoff2017; Di Biase & Hanssen Reference Di Biase and Hanssen2021). These contaminations could also be due to industries, especially agri-food industries, if their effluents are not properly treated, or to wildlife, especially poultry (Yahya et al. Reference Yahya, Blanch, Meijer, Antoniou, Hmaied and Ballesté2017; Edge et al. Reference Edge, Boyd, Shum and Thomas2021). Indeed, the lack of a solid and liquid waste collection and treatment system in the city of Kribi is conducive to the deposition of sediment, which would promote the development of microorganisms that would be evacuated to the beaches during rainy episodes.

In the city of Kribi, wastewater disposal is generally done individually. That which is produced by households is discharged into the environment. Apart from a few homes that have modern cesspits (about 15%), most people pour their wastewater into the yard or into poorly equipped traditional latrines in the open. The flatness of the land and the presence of multiple geomorphologic depressions result in that domestic wastewater being discharged into nature, obviously without any treatment, creating numerous stagnation points where a string of pathogenic microorganisms, parasites, and infectious disease vectors develop (Assako Assako et al. Reference Assako Assako, Tonmeu Djilo, Bley, Vernazza-Licht, Gruénais and Bley2010). As for hotels, generally located on the coast, their septic tanks are emptied by private emptying companies from Douala. This waste is taken to the Bois des Singes wastewater dump in Douala, although it is not impossible that some of these trucks are emptied into the rivers (Nyong, Kienké) that cross the Kribi-Douala road (Assako Assako Reference Assako Assako and Bley2005).

Bathing in water of poor microbiological quality, such as that of the Kribi beaches, thus presents health risks and can lead to infections, mainly gastroenteritis, with varying severity depending on the helminths involved and the concentration of helminth eggs or larvae in the medium (WHO 2006; Saingam et al. Reference Saingam, Li and Yan2020). In rare cases, contaminated water can also lead to more serious infectious diseases such as typhoid, cholera, etc. (WHO 2006; 2021). In addition to the health issue, water contamination by helminth eggs or larvae is also an economic issue, since it can lead to the downgrading, or even the closure, of bathing or recreational fishing areas and thus impact tourism to a greater or lesser extent (Martínez et al. Reference Martínez, Intralawan, Vázquez, Pérez-Maqueo, Sutton and Landgrave2007).

Conclusion

The main objective of this study was to evaluate the influence of tides on the dissemination of intestinal helminths in the waters of the seaside town beaches of Kribi. It was found that the waters of the beaches surveyed are subject to microbiological pollution because they concentrate large quantities of helminth larvae or eggs. This high concentration, which is more pronounced at low tide than at high tide, has potential public health significance. If the developed countries have been able to set up sanitation systems that are still to be perfected, it should be noted that in African cities, in particular Kribi (Cameroon), the issue of efficient waste management in general and wastewater in particular should represent a major concern for the authorities and the populations. To limit microbiological and parasitic pollution of the Kribi beaches, it is urgent that municipal authorities define and implement an efficient plan for the collection and treatment of solid and liquid waste.

Acknowledgments

Paul Alain Nana thanks Professor Ousmane Traoré of Clermont-Ferrand University Hospital Centre for his logistical support.

Financial support

This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

Competing interest

The authors declare none.

Ethical standard

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals.

References

Ajeagah, GA, Foto Menbohan, S, Talom, SN, Ntwong, MM, Tombi, J, Nola, M, Njine, T (2014). Physicochemical and dynamic property of abundance of the intestinal forms of dissemination of the helminths in worn water and from surface in Yaounde (Cameroun). European Journal of Scientific Research 120, 4463.Google Scholar
Ajeagah, GA, Fotseu Kouam, AL (2019). Dissemination of the resistant forms of intestinal worms in the marshy areas of the city of Yaounde (Cameroon): importance of some abiotic factors of the medium. Applied Water Science 9, 19. https://doi.org/10.1007/s13201-019-0895-y.Google Scholar
APHA (2017). Standard Methods for the Examination of Water and Wastewater, 22nd edn. Washington, DC: American Public Health Association.Google Scholar
Assako Assako, RJ (2005). Problématique de l’estimation de la qualité de vie dans un front d’urbanisation en Afrique : Le cas du Bois des Singes à Douala (Cameroun). In Bley, D. (éd.) Cadre de Vie et Travail: Les Dimensions d’une Qualité de Vie au Quotidien. Aix-en-Provence. Éditions Edisud, 6585.Google Scholar
Assako Assako, RJ, Tonmeu Djilo, CA, Bley, D (2010). Risques sanitaires et gestion des eaux usées et des déchets à Kribi (Cameroun). In Vernazza-Licht, N, Gruénais, M, Bley, D (eds), Sociétés, Environnements, Santé. Marseille: IRD Éditions, 257285. https://doi.org/10.4000/books.irdeditions.3620.CrossRefGoogle Scholar
Badri, M, Olfatifar, M, Wandra, T, Budke, CM, Mahmoudi, R, Abdoli, A, Hajialilo, E, Pestehchian, N, Ghaffarifar, F, Foroutan, M, Hashemipour, S, Sotoodeh, S, Samimi, R, Eslahi, AV (2022). The prevalence of human trichuriasis in Asia: A systematic review and meta-analysis. Parasitology Research 121, 1, 110. https://doi.org/10.1007/s00436-021-07365-8.CrossRefGoogle Scholar
Basili, M, Campanelli, A, Frapiccini, E, Marco Lunaa, G, Queroa, GM (2021) Occurrence and distribution of microbial pollutants in coastal areas of the Adriatic Sea influenced by river discharge. Environmental Pollution 285, 117672. https://doi.org/10.1016/j.envpol.2021.117672.CrossRefGoogle ScholarPubMed
Bonadonna, L, Briancesco, R, Suffredini, E, Coccia, A, Della Libera, S, Carducci, A, Verani, M, Federigi, I, Iaconelli, M, Bonanno Ferraro, G, Mancini, P, Veneri, C. Ferretti, E, Lucentini, L, Gramaccioni, L, La Rosa, G (2019), Enteric viruses, somatic coliphages and Vibrio species in marine bathing and non-bathing waters in Italy. Marine Pollution Bulletin 149, 110570. https://doi.org/10.1016/j.marpolbul.2019.110570.CrossRefGoogle ScholarPubMed
Coello Peralta, RD, Salazar Mazamba, ML, Pazmiño Gómez, BJ, Cushicóndor Collaguazo, DM, Gómez Landires, EA, Ramallo, G (2023). Hymenolepiasis Caused by Hymenolepis nana in Humans and Natural Infection in Rodents in a Marginal Urban Sector of Guayaquil, Ecuador. American Journal of Case Reports 24, e939476. https://doi.org/10.12659/AJCR.939476.CrossRefGoogle Scholar
Collender, PA, Kirby, AE, Addiss, DG, Freeman, MC, Remais, JV (2015). Methods for quantification of soil-transmitted helminths in environmental media: current techniques and recent advances. Trends in Parasitology 31, 12, 625–39. https://doi.org/10.1016/j.pt.2015.08.007.CrossRefGoogle ScholarPubMed
Dang, H, Lovell, CR (2016). Microbial surface colonization and biofilm development in marine environments. Microbiology and Molecular Biology Reviews 80, 1, 91138. https://doi.org/10.1128/MMBR.00037-15.CrossRefGoogle ScholarPubMed
Di Biase, V, Hanssen, RF (2021). Environmental strain on beach environments retrieved and monitored by spaceborne synthetic aperture radar. Remote Sensing 13, 21, 4208. https://doi.org/10.3390/rs13214208.CrossRefGoogle Scholar
Edge, TA, Boyd, RJ, Shum, P, Thomas, JL (2021). Microbial source tracking to identify fecal sources contaminating the Toronto Harbour and Don River watershed in wet and dry weather. Journal of Great Lakes Research 47, 2, 366377. https://doi.org/10.1016/j.jglr.2020.09.002.CrossRefGoogle Scholar
Ferrarin, C, Penna, P, Penna, A, Spada, V, Ricci, F, Bilić, J, Krzelj, M, Ordulj, M, Šikoronja, M, Đuračić, I, Iagnemma, L, Bućan, M, Baldrighi, E, Grilli, F, Moro, F, Casabianca, S, Bolognini, L, Marini, M (2021). Modelling the quality of bathing waters in the Adriatic Sea. Water 13, 11, 1525. https://doi.org/10.3390/w13111525.CrossRefGoogle Scholar
Fotseu Kouam, AL, Ajeagah, GA (2019). Dissemination of the resistant forms of intestinal worms in the marshy areas of the city of Yaounde (Cameroon): Importance of some abiotic factors of the medium. Applied Water Science 9, 19. https://doi.org/10.1007/s13201-019-0895-y.Google Scholar
Guilavogui, T, Verdun, S, Koïvogui, A, Viscogliosi, E, Certad, G (2023). Prevalence of intestinal parasitosis in Guinea: Systematic review of the literature and meta-analysis. Pathogens 12, 2, 336. https://doi.org/10.3390/pathogens12020336.CrossRefGoogle ScholarPubMed
Holland, C, Sepidarkish, M, Deslyper, G, Abdollahi, A, Valizadeh, S, Mollalo, A, Mahjour, S, Ghodsian, S, Ardekani, A, Behniafar, H, Gasser, RB, Rostami, A (2022). Global prevalence of Ascaris infection in humans (2010–2021): A systematic review and meta-analysis. Infectious Diseases of Poverty 11, 1, 113. https://doi.org/10.1186/s40249-022-01038-z.CrossRefGoogle ScholarPubMed
Ikumapayi, UN, Sanyang, C, Pereira, DI (2019). A case report of an intestinal helminth infection of human Hymenolepiasis in rural Gambia. Clinical Medical Reviews and Case Reports 6, 1, 251. https://doi.org/10.23937/2378-3656/1410251.Google ScholarPubMed
Kucik, CJ, Martin, GL, Sortor, BV (2004). Common intestinal parasites. American Family Physician 69, 5, 11611168.Google ScholarPubMed
Kraus, R, Baljak, V, Vukić Lušić, D, Kranjčević, L, Cenov, A, Glad, M, Kauzlarić, V, Lušić, D, Grbčić, L, Alvir, M, Pećarević, M, Jozić, S (2022). Impacts of atmospheric and anthropogenic factors on microbiological pollution of the recreational coastal beaches neighboring shipping ports. International Journal of Environmental Research and Public Health 19, 14, 8552. https://doi.org/10.3390/ijerph19148552.CrossRefGoogle ScholarPubMed
Lupia, T, Crisà, E, Gaviraghi, A, Rizzello, B, Di Vincenzo, A, Carnevale-Schianca, F, Caravelli, D, Fizzotti, M, Tolomeo, F, Vitolo, U, De Benedetto, I, Shbaklo, N, Cerutti, A, Fenu, P, Gregorc, V, Corcione, S, Ghisetti, V, De Rosa, FG (2023). Overlapping infection by Strongyloides spp. and Cytomegalovirus in the immunocompromised host: A comprehensive review of the literature. Tropical Medicine and Infectious Disease 8, 7, 358. https://doi.org/10.3390/tropicalmed8070358.CrossRefGoogle ScholarPubMed
Madani, M, Seth, R, Leon, LF, Valipour, R, McCrimmon, C (2020). Three dimensional modelling to assess contributions of major tributaries to fecal microbial pollution of lake St. Clair and Sandpoint Beach. Journal of Great Lakes Research 46, 1, 159179. https://doi.org/10.1016/j.jglr.2019.12.005.CrossRefGoogle Scholar
Manezeu Tonleu, EO, Nana, PA, Onana, FM, Nyamsi Tchatcho, NL, Tchakonté, S, Nola, M, Sime-Ngando, T, Ajeagah Aghaindum, G (2021). Evaluation of the health risks linked to two swimming pools regularly frequented from the city of Yaounde in Cameroon (Central Africa). Environmental Monitoring and Assessment 193, 36. https://doi.org/10.1007/s10661-020-08829-7.CrossRefGoogle ScholarPubMed
Manini, E, Baldrighi, E, Ricci, F, Grilli, F, Giovannelli, D, Intoccia, M, Casabianca, S, Capellacci, S, Marinchel, N, Penna, P, Moro, F, Campanelli, A, Cordone, A, Correggia, M, Bastoni, D, Bolognini, L, Marini, M, Penna, A (2022). Assessment of spatio-temporal variability of faecal pollution along coastal waters during and after rainfall events. Water 14, 3, 502. https://doi.org/10.3390/w14030502.CrossRefGoogle Scholar
Manz, KM, Clowes, P, Kroidl, I, Kowuor, DO, Geldmacher, C, Ntinginya, NE, Maboko, L, Hoelscher, M, Saathoff, E (2017). Trichuris trichiura infection and its relation to environmental factors in Mbeya region, Tanzania: A cross-sectional, population-based study. PLoS One 12, 4, e0175137. https://doi.org/10.1371/journal.pone.0175137.CrossRefGoogle ScholarPubMed
Martínez, ML, Intralawan, A, Vázquez, G, Pérez-Maqueo, O, Sutton, P, Landgrave, R (2007). The coasts of our world: Ecological, economic and social importance. Ecological Economics 63, 254272. https://doi.org/10.1016/j.ecolecon.2006.10.022.CrossRefGoogle Scholar
Mohammed, RL, Echeverry, A, Stinson, CM, Green, M, Bonilla, TD, Hartz, A, McCorquodale, DS, Rogerson, A, Esiobu, N (2012). Survival trends of Staphylococcus aureus, Pseudomonas aeruginosa, and Clostridium perfringens in a sandy South Florida beach. Marine Pollution Bulletin 64, 6, 12011209. https://doi.org/10.1016/j.marpolbul.2012.03.010.CrossRefGoogle Scholar
Nana, PA, Pahane Mbiada, M, Tchakonté, S, Moche, K, Mouchili Palena, RS, Nola, M, Sime-Ngando, T (2023a). Influence of seasons and tides on the distribution of enteric protozoa on the shores of the Atlantic Ocean in Kribi (South Region of Cameroon): Health risks related to bathing. Pollutants 3, 2, 243254. https://doi.org/10.3390/pollutants3020018.CrossRefGoogle Scholar
Nana, PA, Ebonji Seth, R, Ndjuissi Tamko, NA, Onambélé Ossomba, VR, Bricheux, G, Metsopkeng, CS, Nola, M, Sime-Ngando, T (2023b). Tidal effect on the dispersion of fecal pollution indicator bacteria and associated health risks along the Kribi beaches (Southern Atlantic coast, Cameroon). Regional Studies in Marine Science 60, 102831. https://doi.org/10.1016/j.rsma.2023.102831.CrossRefGoogle Scholar
Ngoma, D, Wang, Y (2018). Hhaynu micro hydropower scheme: Mbulu – Tanzania comparative river flow velocity and discharge measurement methods. Flow Measurement and Instrumentation 62, 135142. https://doi.org/10.1016/j.flowmeasinst.2018.05.007.CrossRefGoogle Scholar
Nimnoi, P, Pongsilp, N (2020). Marine bacterial communities in the upper gulf of Thailand assessed by Illumina next-generation sequencing platform. BMC Microbiology 20, 111. https://doi.org/10.1186/s12866-020-1701-6.CrossRefGoogle ScholarPubMed
Oduro, D, Darko, S, Blankson, ER, Mensah, GI (2023). Assessment of bacteria contaminants in different zones and point sources of sandy beaches in Accra, Ghana. Microbiology Insights 16, 18. https://doi.org/10.1177/11786361231195152.CrossRefGoogle ScholarPubMed
Olivry, JC (1986). Fleuves et rivières du Cameroun. In Collection Monographies Hydrologiques, No. 9. Paris: ORSTOM, 733.Google Scholar
Rodier, J, Legube, B, Merlet, N (2009). The Water Analysis, 9th Edition. Paris: Dunod, 1579.Google Scholar
Rodríguez, J, Gallampois, CMJ, Haglund, P, Timonen, S, Rowe, O (2021). Bacterial communities as indicators of environmental pollution by POPs in marine sediments. Environmental Pollution 268, 115690. https://doi.org/10.1016/j.envpol.2020.115690.CrossRefGoogle ScholarPubMed
Saingam, P, Li, B, Yan, T (2020). Fecal indicator bacteria, direct pathogen detection, and microbial community analysis provide different microbiological water quality assessment of a tropical urban marine estuary. Water Research 185, 116280. https://doi.org/10.1016/j.watres.2020.116280.CrossRefGoogle ScholarPubMed
Schiefke, I, Schmäschke, R, Ott, R, Schiefke, F, Mössner, J, Schubert, S (2006). Einheimische Helminthosen [Indigenous helminthiasis]. Internist (Berl) 47, 8, 793794, 796, 798–800. https://doi.org/10.1007/s00108-006-1660-5.CrossRefGoogle Scholar
Schär, F, Trostdorf, U, Giardina, F, Khieu, V, Muth, S, Marti, H, Vounatsou, P, Odermatt, P (2013). Strongyloides stercoralis: Global distribution and risk Factors. PLOS Neglected Tropical Diseases 7, 7, e2288. https://doi.org/10.1371/journal.pntd.0002288.CrossRefGoogle ScholarPubMed
Silver, ZA, Kaliappan, SP, Samuel, P, Venugopal, S, Kang, G, Sarkar, R, Ajjampur, SSR (2018). Geographical distribution of soil transmitted helminths and the effects of community type in South Asia and South East Asia – A systematic review. PLOS Neglected Tropical Diseases 12, 1, e0006153. https://doi.org/10.1371/journal.pntd.0006153.CrossRefGoogle ScholarPubMed
Soto-Varela, ZE, Rosado-Porto, D, Bolívar-Anillo, HJ, Pichón González, C, Granados Pantoja, B, Estrada Alvarado, D, Anfuso, G (2021). Preliminary microbiological coastal water quality determination along the Department of Atlántico (Colombia): Relationships with beach characteristics. Journal of Marine Science and Engineering 9, 2, 122. https://doi.org/10.3390/jmse9020122.CrossRefGoogle Scholar
Suwansaksri, J, Nithiuthai, S, Wiwanitkit, V, Soogarun, S, Palatho, P (2002). The formol-ether concentration technique for intestinal parasites: comparing 0.1 N sodium hydroxide with normal saline preparations. The Southeast Asian Journal of Tropical Medicine and Public Health 33, Suppl 3, 9798.Google ScholarPubMed
Thivierge, K (2014). Identification Morphologique des Parasites Intestinaux. Quebec: Cahier de Stage, Institut National de Santé, 58.Google Scholar
Truscott, JE, Turner, HC, Farrell, SH, Anderson, RM (2016). Soil-transmitted helminths: Mathematical models of transmission, the impact of mass drug administration and transmission elimination criteria,. Advances in Parasitology 94, 133198. https://doi.org/10.1016/bs.apar.2016.08.002.CrossRefGoogle ScholarPubMed
Walusimbi, B, Lawson, MAE, Nassuuna, J, Kateete, DP, Webb, EL, Grencis, RK, Elliott, AM (2023). The effects of helminth infections on the human gut microbiome: A systematic review and meta-analysis. Frontiers in Microbiomes 2, 1174034. https://doi.org/10.3389/frmbi.2023.1174034.CrossRefGoogle Scholar
Weiskerger, CJ, Brandão, J, Ahmed, W, Aslan, A, Avolio, L, Badgley, BD, Boehm, AB, Edge, TA, Fleisher, JM, Heaney, CD, Jordao, L, Kinzelman, JL, Klaus, JS, Kleinheinz, GT, Meriläinen, P, Nshimyimana, JP, Phanikumar, MS, Piggot, AM, Pitkänen, T, Robinson, C, Sadowsky, MJ, Staley, C, Staley, ZR, Symonds, EM, Vogel, LJ, Yamahara, KM, Whitman, RL, Solo-Gabriele, HM, Harwood, VJ (2019). Impacts of a changing earth on microbial dynamics and human health risks in the continuum between beach water and sand. Water Research 162, 456470. https://doi.org/10.1016/j.watres.2019.07.006.CrossRefGoogle ScholarPubMed
WHO (2006). Guidelines for safe recreational water environments. Volume 2, Swimming pools and similar environments. Available at http://www.who.int/iris/handle/10665/43336 (accessed 02 january 2024).Google Scholar
WHO (2019). Bench aids for the diagnosis of intestinal parasites, 2nd ed. Available at https://www.who.int/publications/i/item/9789241515344 (accessed 02 january 2024).Google Scholar
WHO (2021). Guidelines on recreational water quality. Volume 1: Coastal and fresh waters. Available at https://www.who.int/publications/i/item/9789240031302 (accessed 02 january 2024).Google Scholar
Yahya, M, Blanch, AR, Meijer, WG, Antoniou, K, Hmaied, F, Ballesté, E (2017). Comparison of the performance of different microbial source tracking markers among European and North African Regions. Journal of Environmental Quality 46, 4, 760766. https://doi.org/10.2134/jeq2016.11.0432.CrossRefGoogle ScholarPubMed
Figure 0

Figure 1. Location map showing sampling points.

Figure 1

Table 1. Some hydrodynamic characteristics of the surveyed sites

Figure 2

Figure 2. Physicochemical variables according to seasons and tidal cycles. SRS: Short Rainy Season; SDS: Short Dry Season; LRS: Long Rainy Season; LDS: Long Dry Season.

Figure 3

Table 2. Helminth eggs or larvae abundance recorded in the different sites

Figure 4

Figure 3. Helminth eggs or larvae abundanceaccording to seasons and tidal cycles. (A) Hymenolepis nana; (B) Strongyloides sp.; (C) Ascaris sp.; (D) Ancylostoma duodenale; (E) Trichuris trichiura. SRS: Short Rainy Season; SDS: Short Dry Season; LRS: Long Rainy Season; LDS: Long Dry Season.