Hymenolepis nana is responsible for many parasitic infections in tropical areas, with its persistence in aquatic environments as major contributory factor. A study aimed at demonstrating the effectiveness of some disinfectants on the viability of Hymenolepis nana eggs was conducted in microcosm. Sampling consisted of taking wastewater and sewage sludge samples in sterilized containers and then transporting to the laboratory of Hydrobiology and Environmental Sciences for the determination of Hymenolepis nana eggs using standard protocols. The experimental set-up consisted of five replicates, four tests and a control. The test samples were successively treated with four disinfectants (calcium chlorite, hydrogen peroxide, gypsum and sodium hypochlorite). The physico-chemical parameters were measured before and after disinfection. The samples were then observed under an optical microscope after concentration of the sample through sedimentation and McMaster technique. The viability of the eggs was determined using incubation and staining techniques. The analysis revealed that the selected disinfectants significantly reduced the physico-chemical parameters (with an average yield ranging from 79.24 ± 19.43% to 99.24 ± 1.47%). These physico-chemical parameters can significantly influence the treatment of Hymenolepis nana eggs either by absorbing the disinfectant or by constituting a protective barrier for the eggs, and the physico-chemical nature of the disinfectant strongly influences the formation of disinfection by-products. Calcium chlorite showed a greater effectiveness in reducing egg viability with efficiency rates of 93.12 ± 9.12% followed by hydrogen peroxide (89.57 ± 14.55%), sodium hypochlorite (82.51 ± 14.39%) and gypsum (80.85 ± 12.88%). The results obtained with gypsum are almost similar to those obtained with other disinfectants (calcium chlorite, hydrogen peroxide and sodium hypochlorite) and clearly show that this disinfectant can be used in water treatment because, unlike other chemical disinfectants, it has no known toxic effects.

  • The eggs isolated are highly resistant to the different disinfectants used for water treatment and their inactivation depends on the physico-chemical nature of the water.

  • Gypsum had very significant effects on the inactivation of eggs and could well be used as an alternative for water treatment, as it does not present toxic effects, unlike other chemical disinfectants assessed.

Globally, more than 1 billion people are infected with helminth eggs that are transmitted through water or soil (Crompton 2008; Bagayan et al. 2015). The largest number of helminth cases is observed in Africa (193 million), the majority of which are children under 15 years of age (Jimenez-Cisneros & Maya-Rendon 2007; Adu-Gyasi et al. 2018). In Cameroon, helminthiases are among the most chronic parasitic diseases (Tchuem Tchuemté et al. 2001). Most helminthiases are contracted through the consumption of contaminated water and food. This pollution is generally from faecal origin (Keraita & Amoah 2011). This strong preponderance is also due to the resistance of some helminth species to disinfectants commonly used in wastewater treatment. This resistance is due to the very hard outer shell and basic structure (Klutse & Baleux 2009; Bandala et al. 2012). In wastewater, pathogens of bacterial or viral origin do not survive for long when exposed to high temperatures, whereas helminth eggs are endowed with a high resistance that can exceed several years in nature (Ibañez-Cervantes et al. 2013). The presence of helminth eggs in sewage sludge and wastewaters increases the risk of infestation directly to humans or indirectly through the reuse of sludge for agricultural purposes (WHO 1989), especially if the eggs are ingested at an infestive stage (WHO 2006). To control the spread of helminthiasis, WHO has developed treatment devices for geohelminths, particularly schistosomiasis using praziquantel (WHO 2011). However, few data are available on the treatment of hymenolepiasis, which is an infection caused by Hymenolepis nana, and is considered to be the most widespread human cestode in the world (Magalhaes Soares et al. 2013), causing 50–75 million infections (Khudair et al. 2017) with prevalences ranging from 3.22% to 21% in children (Acha & Szyfres 2003; Bagayan et al. 2015). This infection is manifested by abdominal pain, fever, vomiting and diarrhoea (Panti-May et al. 2020). Hymenolepis nana is a cosmopolitan parasite that is widespread in developing countries and in countries with warm climates (Roberts & Janovy 2008; Malheiros et al. 2014). Studies carried out in many regions in the world, including the USA (Merward et al. 2011; Starr & Montgomery 2011), Pakistan (Hall & Kirby 2010) and Bangladesh (Karim et al. 2018), have reported the presence of this parasite. However, it is mainly endemic in Africa (CDC 2015). Studies on the diagnosis of Hymenolepis have been carried out in Ethiopia (Nguyen et al. 2012), Nigeria (Adenusi & Adewoga 2013) and Cameroon (Ajeagah & Fotseu 2019), and Hymenolepis was found at very high densities. Hymenolepis eggs can remain viable in tropical climates for up to 12 months (Sanguinetti et al. 2005). Also, the Hymenolepis eggs tend to develop in areas with poor socio-structural conditions and in water bodies (Fitte et al. 2018). Contaminated wastewater is a permanent means of transmission of Hymenolepis infections. Studies carried out in the treatment of this parasite have mainly focused on parasites isolated from excreta or faeces (Kone et al. 2007; McKay 2010; Merward et al. 2011; Adenusi & Adewoga 2013; Jirků et al. 2018; Řežábková et al. 2019). Few studies are available on the treatment of Hymenolepis eggs in wastewater. However, this parasite acquires its virulence during the passage of the eggs in aquatic environment, making water treatment more complex. Treatment by sedimentation and solar disinfection are techniques commonly used in wastewater treatment plants and faecal sludge; these techniques are sometimes inappropriate because some parasites accumulate for a long time in sedimentation tanks and can keep their viability, and moreover, during the treatment by solar radiation, their DNA can be reactivated if the intensity of the radiation used is not optimal (Keffala et al. 2012). This study was carried out with a view to highlight in microcosm the efficiency of some disinfectants (calcium hypochlorite, sodium hypochlorite, hydrogen peroxide and gypsum) on the viability of Hymenolepis nana eggs isolated from wastewater and sewage sludge in Yaoundé and its surroundings and to assess the influence of physico-chemical parameters on the efficiency of the disinfectants. More specifically, the aim was to carry out a physico-chemical analysis of wastewater and faecal sludge, to conduct a morphological analysis of Hymenolepis nana eggs and to evaluate in microcosm the effectiveness of some disinfectants (calcium chlorite, hydrogen peroxide, gypsum and sodium hypochlorite) on the viability of Hymenolepis nana eggs.

Study framework and sampling stations

This study took place from June 2018 to June 2019 and was carried out in two phases. The first phase, which lasted 3 months (June to August), consisted of a series of screening tests to determine the ranges of minimum observable effect concentrations on eggs. At the end of this screening, four disinfectants (calcium hypochlorite, sodium hypochlorite, hydrogen peroxide and gypsum) and six ranges of mass concentrations were obtained for the analyses, namely (0.1 g/L, 0.2 g/L, 0.3 g/L, 0.4 g/L, 0.5 g/L and 0.6 g/L) for calcium chloride and gypsum, and (0.1 cl/L, 0.2 cl/L, 0.3 cl/L, 0.4 cl/L, 0.5 cl/L and 0.6 cl/L) for hydrogen peroxide and sodium chloride.

Description of sampling stations

The wastewater samples were collected from the effluents of the Central Prison, the University City, and the Sic Biyem-Assi Camp. These effluents from social housing and homes are rich in human excreta (pathogenic microorganisms), nutrients and organic matter. The faecal sludge was collected from a faecal sludge station in Nomayos. This sludge, which is relatively concentrated in pathogens, comes from public toilets and homes and is biochemically unstable. These sites are described in detail below.

Central Prison (CP)

Yaounde Central prison is the largest prison in Cameroon, with geographical coordinates of 3°51′53.0″N and 11°28′37.3″E, and an altitude of 679 m. This prison is currently faced with overcrowding, which also leads to an overproduction of faecal matter, which is permanently evacuated to the outside with the liquid effluent through the canal that borders the rear side of this prison.

University City (CU)

With geographical coordinates of 4°00′20.2″N and 09°42′54.4″E and an altitude of 644 m, the students' residence of the University of Yaounde I is the largest university city in Cameroon and is home to thousands of students. This campus generates a large quantity of wastewater and faecal matter, which are connected to an underground canal, allowing it to be conveyed to a treatment plant of the biofilters. This plant is currently non-functional, and this water ends up directly in nature without treatment. The samples for this study were taken from an aerated water channel.

Camp Sic Biyem-Assi (BA)

With geographical coordinates 04°28′18.6″N and 11°53′31.4″E and an altitude of 637 m, this Sic camp is among the largest social housing in Yaounde and is home to several thousand people. The wastewater produced by the users is sent to the filter bed wastewater purification station. Samples for analysis were taken from a wastewater aerated water channel before the water arrives at the treatment plant.

Discharge of Nomayos (No)

With geographical coordinates 04°09′33.7″N and 11°22′08.9″E and an altitude of 629 m, the Nomayos sewage sludge discharge station is located on the periphery of Yaounde. For the time being, it is the sole discharge point for sewage sludge removed from the septic tanks of households in this area. Trucks unload their contents on a surface assigned to them by the local authorities, and these discharges generally end up in downstream waterways. The population living in the vicinity of this site practise food and market gardening and use the sludge from these excreta as fertilizer. The sludge collected consisted of a mixture of relatively concentrated black urine and faeces, stored for a few days, biochemically unstable, coming from homes and public toilets.

Preparation of disinfectant solutions

Calcium chloride (CaCl2) and gypsum (CaSO4·2H2O)

Calcium chloride (CaCl2) is a disinfectant commonly used to treat water intended for consumption, particularly water from wells, springs and boreholes. Gypsum (CaSO4·2H2O) is present in nature; it is a soft saline rock often used for water purification due to its high flocculating power. The fine crystals of CaCl2 and (CaSO4·2H2O) used for this study were weighed using a Sartorius balance at different concentrations (0.1 mg/L; 0.2 mg/L; 0.3 mg/L; 0.4 mg/L; 0.5 mg/L and 0.6 mg/L); these concentrations were used for the treatment of Hymenolepis nana eggs.

Sodium hypochlorite (NaClO) and hydrogen peroxide (H2O2)

Sodium hypochlorite (NaClO), commonly known as bleach, is the disinfectant most commonly used for the treatment and purification of water. The hydrogen peroxide used for this study is Solvay branded and has a concentration of 30%. It is readily available on the market and regularly used in industry for water treatment. The volume concentrations used (0.1 cl/L, 0.2 cl/L, 0.3 cl/L, 0.4 cl/L, 0.5 cl/L and 0.6 cl/L) were measured using test tubes and graduated pipettes, and these different volumes were introduced into the samples to be processed.

Sampling

Sampling of wastewater and sewage sludge was carried out instantly following the recommendations of Rodier (2009) for physico-chemical analysis and following the approach proposed by Keffala et al. (2012) for biological analysis. Samples were collected using sterile 5 L bottles and returned to the laboratory. For wastewater, sampling was done directly on the effluent. For sewage sludge, the sample was taken directly after discharge by trucks.

Physico-chemical analyses and determination of helminth eggs

Physico-chemical analyses

The physico-chemical parameters evaluated in this study were measured using conventional techniques described by APHA (2005) and Rodier (2009) with appropriate reagents. The pH was measured using a multiparameter HANA HI 9829. Suspended solids and turbidity were measured colorimetrically on the HACH DR 2900 spectrophotometer at wavelengths λ = 810 nm and λ = 450 nm for suspended solids and turbidity, respectively. After calibration of the instrument, a 10 mL spectrophotometric cell containing the sample was inserted into the spectrophotometer. The suspended solids and turbidity contents were expressed in mg/L and formazin turbidity units (FTU), respectively. Measurements of nitrate and ammoniacal nitrogen contents in mg/L of water were determined by colorimetry, using the HACH DR/3900 spectrophotometer. The reagents used were Nitraver for nitrate, Nessler and Rochelle salt for ammoniacal nitrogen. The oxidability contents in mg/L of KMnO4 were measured by volumetry. Organic matter was determined by oxidability, because some chemical disinfectants could influence the determination of organic matter on the test samples when using chemical oxygen demand (COD).

Determination of helminth eggs

Sample pre-treatment

The sample brought back to the laboratory was sieved for the removal of large particles, and then the viable eggs in the sample were previously quantified, and non-viable eggs were removed by flotation with n-butanol. Approximately 1 mL of n-butanol was added to 500 mL of sample to allow the non-viable eggs, which are less dense, to float; then these non-viable eggs were removed by suction of the supernatant.

Disinfection test

For the treatment and disinfection of the samples, we made a device comprising four series of six Erlenmeyer flasks (each series of six Erlenmeyer flasks corresponding to the six concentration ranges of each disinfectant), and then 500 mL of previously homogenized sample was introduced into each Erlenmeyer flask. Each disinfectant was introduced into a series of four Erlenmeyer flasks at the different concentrations (C1, C2, C3, C4, C5, C6). The samples were then homogenized using a magnetic device and a baro-magnet to ensure perfect contact between the disinfectant and the sample. To allow the disinfectant to act, a contact time of 24 hours was observed for each sample (Akam et al. 2005). Then 5 mL of pellet was taken from each sample and introduced into a test tube; this pellet was then washed with sterile water twice (Amoah et al. 2017a). To this 5 mL of pellet was added 5 mL of distilled water, and it was shaken and centrifuged at 500 rpm for 7 min (Ibañez-Cervantes et al. 2013). The supernatant from this centrifugation was removed by aspiration. The resulting pellet was washed a second time with sodium thiosulphate solution to neutralize any excess disinfectant. The resulting pellet was subjected to viability testing by staining and incubation, after concentration of the eggs by sedimentation and McMaster technique. The test was repeated for all sampling campaigns conducted during this study, with observations repeated twice (Khallaayoune & Fatiha 1995).

Viability analysis

Staining viability test
For the staining viability test we used the neutral red, which is a vital dye (Merward et al. 2011; Karkashan et al. 2015). Neutral red is a dye that has the ability to bind to the structure of viable eggs and stain them red. After concentration of the parasitic elements, 1 mL of neutral red was added to each sample, and a contact time of 10 minutes was observed to allow the stain to penetrate the viable eggs. These samples were then placed on the McMaster slides for observation, the eggs stained red by the stain were considered viable, and the unstained eggs were considered potentially non-viable (Sarvel et al. 2006). The number of eggs per litre was calculated using the formula proposed by Sengupta et al. (2011).
formula
where: N = number of eggs per litre of sample; X = volume of final product (mL); A = number of eggs counted on the McMaster slide or average of the numbers found in two or three slides; P = capacity of the McMaster slide (0.3 mL); V = volume of the initial sample (litres).
Incubation viability test
For this technique, 5 mL of pellet was incubated on Petri dishes in an oven at 30 °C for 30 days (Pecsonn et al. 2007); during these days the process of reduction of egg viability was demonstrated, starting from the destruction of the egg membrane to the inactivation of the larva. Then the eggs were examined under light microscopy, so that in non-viable eggs segmentation stopped while viable eggs continued their segmentation and development until larval formation (Stien 1989; Keffala et al. 2012). Eggs with mobile larvae were considered viable (Amoah et al. 2017b). Identification was done through morphological analysis of the size, shape and content of the eggs (Řežábková et al. 2019). Changes in the oncosphere and the hexacanth embryo were revealed by light microscopy using 40× and 100× objectives. Measurements were made using an eyepiece micrometer and photos were taken using an Xploview model photographic device attached to one of the microscope's eyepieces. The number of eggs per litre was calculated using the formula proposed by Ajeagah et al. (2014):
formula
with: Vx = volume of pellet in 1 L of sample, Vy = volume of pellet used for observation, y = number of eggs observed in Vy.

Statistical analysis

The normality of the data was assessed using the Kolmogorov-Smirnov test. The comparisons between the different concentrations (C1, C2, C3, C4, C5, and C6), on the one hand, and between the control value and the values obtained after treatment, on the other hand, were carried out using the ANOVA test and Students' t test. Correlations between physico-chemical parameters and viable eggs counted before and after disinfection were performed using Pearson ‘r’ correlation test. All these analyses were carried out using the SPSS version 17.0 software. The efficiency of the different disinfectants was calculated using the following formula:
formula

Results

Morphological description of Hymenolepis nana eggs and structural modification related to the action of disinfectants

Before incubation the eggs show a typical morphology (Figure 1(a) and 1(b)); characterised by a double membrane allowing protection of the cytoplasmic content and genetic material. After incubation the embryonic mass starts to develop (Figure 1(c)); the egg will follow the process of embryogenesis and after several segmentations it will reach the blastula and then gastrula stage and give a mobile larva after one month of incubation. Eggs exposed to the optimal concentrations for their inactivation will lose their viability, so the outer membrane will be subjected to the oxidizing pressure of the disinfectant and will begin to twist (Figure 1(d)), and then it will crack, increasing the porosity of the egg (Figure 1(e)). As the number of pores on the outer membrane increases, the passage of the disinfectant from the external to the internal environment of the egg will increase. The significant entry of a high concentration of disinfectant will damage the oncosphere and nuclear material and cause inactivation of the egg (Figure 1(f)), and the cytoplasmic contents will be released into the external environment as simple non-pathogenic inclusions (Figure 1(g)). After incubation non-viable eggs contain an immobile larva (Figure 1(h)). After staining, the viable eggs adsorb the red dye (Figure 1(j)), while the non-viable eggs remain colourless (Figure 1(i)).

Figure 1

Image of Hymenolepis nana eggs before incubation (a and b), viable eggs having formed the larva after incubation (c), non-viable eggs having formed the immobile larva after incubation (h), non-viable eggs obtained after incubation (d, e, f and g), non-viable eggs obtained after coloration with the neutral red (i), viable eggs obtained after coloration (j).

Figure 1

Image of Hymenolepis nana eggs before incubation (a and b), viable eggs having formed the larva after incubation (c), non-viable eggs having formed the immobile larva after incubation (h), non-viable eggs obtained after incubation (d, e, f and g), non-viable eggs obtained after coloration with the neutral red (i), viable eggs obtained after coloration (j).

Variation in the number of viable eggs isolated from the Central Prison effluent as a function of disinfectant concentrations

Overall, it was observed that the number of viable eggs gradually decreases as the concentration of disinfectants increases; 601 viable eggs/L (Figure 2(a)) were counted in the control sample. After application of disinfectants, the lowest densities were observed at C6 concentration (16, 27, 61 and 61 eggs/L) for hydrogen peroxide, calcium chloride, gypsum and sodium hypochlorite, respectively. The variation profile of the box-plot graph shows a similar pattern (Figure 2(b)).

Figure 2

Variation in the number of viable eggs identified in the Central Prison effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Figure 2

Variation in the number of viable eggs identified in the Central Prison effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Statistical analysis showed that there is a significant difference between the densities of viable eggs obtained between concentrations C1 and C5 (p = 0.005204), C1 and C6 (p = 0.001552). There was also a significant difference between the control value and the viable egg density obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.002778).

Spatial variation in the number of viable eggs isolated from Nomayos sewage sludge

Before application of the disinfectants 535 viable eggs/L were identified in the control sample (Figure 3(a)). The lowest densities were observed at the C6 concentration (65, 39, 17, 0 eggs/L) for gypsum (65 eggs/L), sodium hypochlorite (39 eggs/L), hydrogen peroxide (17 eggs/L) and calcium chloride (0 eggs/L). Figure 3(b) shows a box-plot graph of the values obtained; it can be seen that only calcium chloride gives complete inactivation of the eggs (0 viable eggs/L), and the other three disinfectants show a similar pattern of variation.

Figure 3

Variation in the number of viable eggs identified on the Nomayos effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Figure 3

Variation in the number of viable eggs identified on the Nomayos effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Statistical analysis revealed that there is a significant difference between the densities of viable eggs obtained between concentrations C1 and C5 (p = 0.04032), C1 and C6 (p = 0.01354). There was also a significant difference between the control value and the viable egg density obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.006543).

Variation in the number of viable eggs isolated from the wastewater of the University Campus of Yaounde I

Before disinfection, 963 viable eggs/L (Figure 4(a)) were identified in the control sample. After application of disinfectants, the lowest densities were observed at C6 concentration (156, 135, 36, 21 eggs/L) for sodium hypochlorite gypsum, hydrogen peroxide and calcium chloride, respectively. Figure 4(b) shows a box-plot graph of the values obtained with the different disinfectants; calcium chloride and hydrogen peroxide were more effective than the other two disinfectants.

Figure 4

Variation in the number of viable eggs identified in the University City effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Figure 4

Variation in the number of viable eggs identified in the University City effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Statistical analysis showed that there is a significant difference between the viable egg densities obtained between the concentrations C1 and C4 (p = 0.0007096), C1 and C5 (p = 0.000102), C1 and C6 (p = 2.33 × 10−5), C2 and C5 (p = 0.007568), C2 and C6 (p = 0.001558), C3 and C4 (p = 0.02057), C3 and C5 (p = 0.002571), C1 and C6 (p = 0.0004888). There was also a significant difference between the control value and the viable egg density obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.003255).

Variation in the number of viable eggs isolated from Camp Sic Biyem-Assi

Before disinfection, 445 viable eggs (Figure 5(a)) were identified in the control sample. The lowest densities were observed at C6 concentration (154, 79, 66, 30 eggs/L) for gypsum, hydrogen peroxide, sodium hypochlorite and calcium chloride, respectively. Figure 5(b) shows the pattern of variation in the pooled values for each disinfectant, with calcium hypochlorite showing better efficacy compared to hydrogen peroxide.

Figure 5

Variation in the number of viable eggs identified on the Biyem-Assi effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Figure 5

Variation in the number of viable eggs identified on the Biyem-Assi effluent (a), box-plot graph of egg density obtained before and after disinfection (b).

Statistical analysis revealed that there is a significant difference between the viable egg densities obtained between concentrations C1 and C4 (p = 0.005662), C1 and C5 (p = 0. 0001971), C1 and C6 (p = 5.87 × 10−6), C2 and C4 (p = 0.02583), C2 and C5 (p = 0.0008993), C2 and C6 (p = 2.34 × 10−5), C3 and C4 (p = 0.08296), C3 and C5 (p = 0.002642), C3 and C6 (p = 5.25 × 10−5), C4 and C6 (p = 0.03788). There was also a significant difference between the control value and the viable egg densities obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.005618).

Variation of physico-chemical parameters

Ammonium (NH+4)

The ammonium content obtained on the effluent from the University City plant before treatment is 16.2 mg/L (Figure 6(a)); after application of disinfectants the lowest value (0.29 mg/L) was obtained on the sample treated with sodium hypochlorite. The control value obtained at the Central Prison plant was 3.5 mg/L (Figure 6(b)); after application of disinfectants the lowest value (0.13 mg/L) was obtained in the sample treated with C6 gypsum. The control value obtained at the Nomayos plant before treatment is 48 mg/L (Figure 6(c)); the lowest value (1.3 mg/L) was obtained for the sample treated with C6 gypsum after application of disinfectants. The control value obtained at the Biyem-Assi plant before treatment is 3.5 mg/L (Figure 6(d)); after application of disinfectants the lowest value (0.9 mg/L) was obtained on the sample treated with sodium hypochlorite at C6 concentration.

Figure 6

Variation in ammonium levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Figure 6

Variation in ammonium levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Statistical analysis showed that there is a significant difference between the ammonium contents obtained between concentrations C1 and C5 (p = 0.008614), C1 and C6 (p = 0.004823). There is also a significant difference between the control value and the nitrogen contents obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.004998).

Nitrate (NO3)

The nitrate concentration obtained on the effluent from the University Campus plant before treatment is 148 mg/L (Figure 7(a)); the values obtained after application of disinfectants fluctuate irregularly. The lowest value (2 mg/L) was obtained on the sample treated with sodium hypochlorite. The control value obtained at the Central Prison plant before treatment is 16.73 mg/L (Figure 7(b)); after application of disinfectants the lowest value (1.1 mg/L) was obtained on the sample treated with gypsum at the C6 concentration. The control value obtained at the Nomayos plant before treatment is 163,840 mg/L (Figure 7(c)); the lowest value (16 mg/L) was obtained on the sample treated with C6 gypsum. The control value obtained at the Biyem-Assi plant before treatment is 3.5 mg/L (Figure 7(d)); after application of disinfectants, the lowest value (0.001 mg/L) was obtained in the sample treated with sodium hypochlorite at the C6 concentration.

Figure 7

Variation in nitrate levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Figure 7

Variation in nitrate levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Statistical analysis revealed that there is no significant difference between the nitrate contents obtained at the different concentrations (p > 0.05). However, there is a significant difference between the control value and the nitrate levels obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.002778).

pH

The pH value obtained on the effluent from the University Campus plant is 7.05 (Figure 8(a)), and the value obtained at Central Prison plant is 8.14 (Figure 8(b)); for these two plants, all values obtained on the samples treated with sodium hypochlorite and calcium chloride are slightly basic, while the values obtained with the samples treated with gypsum and hydrogen peroxide are slightly acidic. The control value obtained at the Nomayos plant before treatment is 7.79 (Figure 8(c)); after application of disinfectants all values obtained on samples treated with calcium hypochlorite tend towards neutrality, while those obtained on samples treated with sodium hypochlorite and hydrogen peroxide were slightly basic and those obtained on samples treated with gypsum were slightly acidic. The control pH value obtained at the Biyem-Assi plant before treatment was slightly acidic, 6.17 (Figure 8(d)); after application of the disinfectants all values obtained for the four disinfectants used at all concentrations tend towards basicity.

Figure 8

Variation of pH levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Figure 8

Variation of pH levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Statistical analysis revealed that there is no significant difference between the pH values obtained at the different concentrations (p > 0.05). However, there is a significant difference between the pH values of the control sample and the values obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.0078).

Turbidity

The turbidity value obtained on the UC plant effluent is 2920 FTU (Figure 9(a)); the lowest turbidity value (130 FTU) was obtained on the gypsum-treated sample after application of disinfectants. The control value obtained at the CP plant before treatment was 3100 FTU (Figure 9(b)); after application of disinfectants the lowest value (19 FTU) was obtained on the gypsum treated sample at the C6 concentration. The control value obtained at the Nomayos station before treatment was 1,884,160 FTU (Figure 9(c)); after application of disinfectants the lowest value (130 FTU) was obtained on the sample treated with hydrogen peroxide at the C6 concentration. The pre-treatment Biyem-Assi plant control value was 560 FTU (Figure 9(d)); the lowest value (210 FTU) was obtained on the sample treated with C6. Statistical analysis showed that there is no significant difference between the turbidity values obtained at the different concentrations (p > 0.05). However, there is a significant difference between the turbidity values of the control sample and the values obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.00454).

Figure 9

Variation of turbidity levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Figure 9

Variation of turbidity levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Suspended solids (SS)

The SS value obtained on the pre-treatment UC effluent was 1,640 mg/L (Figure 10(a)); the lowest value (50 mg/L) was obtained on the gypsum-treated sample. The control value obtained at the pre-treatment CP plant was 1,990 mg/L (Figure 10(b)); the lowest value (20 mg/L) was obtained from the sample treated with hydrogen peroxide at C6 concentration. The control value obtained at Nomayos plant before treatment was 8,600 mg/L (Figure 10(c)). After application of disinfectants, the lowest value (190 mg/L) was obtained on the sample treated with sodium hypochlorite at the C6 concentration. The control value obtained at the Biyem-Assi plant before treatment was 260 mg/L (Figure 10(d)); the lowest value (48 mg/L) was obtained from the sample treated with sodium hypochlorite at C6 concentration after application of disinfectants.

Figure 10

Variation of suspended solids levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Figure 10

Variation of suspended solids levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Statistical analysis revealed that there is no significant difference between the SS values obtained at different concentrations (p > 0.05). However, there is a significant difference between the SS values of the control sample and the values obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.003).

Oxidability

The oxidability value obtained on the pre-treatment UC plant effluent is 148.1 mg/L (Figure 11(a)); the lowest oxidability value (2 mg/L) after application of disinfectants was obtained on the calcium chloride treated sample. The control value obtained at the pre-treatment CP plant is 69.1 mg/L (Figure 11(b)); the lowest value (1.78 mg/L) was obtained in the C6 gypsum-treated sample after application of disinfectants. The control value obtained at Nomayos plant before treatment was 450 mg/L (Figure 11(c)). After application of disinfectants the lowest value (3.6 mg/L) was obtained on the sample treated with gypsum at the C6 concentration. The control value obtained at the Biyem-Assi plant before treatment was 209 mg/L (Figure 11(d)); the lowest value (10.2 mg/L) was obtained on the sample treated with calcium hypochlorite at C6.

Figure 11

Variation of oxidability levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Figure 11

Variation of oxidability levels measured before and after disinfection, University City (a), Central Prison (b), Nomayos (c), Biyem-Assi (d).

Statistical analysis showed that there is a significant difference between the oxidisable matter contents obtained between the concentrations C1 and C4 (p = 0.00146), C1 and C5 (p = 0.002514), C1 and C6 (p = 0.001789), C2 and C5 (p = 0.03906), C2 and C6 (p = 0.0283), C3 and C5 (p = 0.04721), C3 and C6 (p = 0.03374). There was also a significant difference between the control value of oxidisable matter and those obtained after treatment with gypsum, hydrogen peroxide, calcium chloride and sodium hypochlorite (p = 0.004075).

Effectiveness of disinfectants on microorganisms and physico-chemical quality

Table 1 shows the average efficiency yields obtained with different disinfectants at the C6 concentration. Overall, calcium chloride is the most effective disinfectant, inactivating over 93% of the eggs (93.12 ± 9.12%), followed by hydrogen peroxide (89.57 ± 14.55%), sodium hypochlorite (82.51 ± 14.39%), and gypsum (80.85 ± 12.88%). For physico-chemical parameters, the best abatement efficiencies of ammonia nitrogen (95.46 ± 1.93%) and nitrate (99.24 ± 1.47%) were obtained on the sample treated with sodium hypochlorite. Gypsum provided the greatest efficiency in reducing suspended solids (90.72 ± 11.39%), turbidity (87.18 ± 16.77%) and oxidizable materials (97.21 ± 3.3%).

Table 1

Efficiency of disinfectants on Hymenolepis nana eggs and some physico-chemical parameters of wastewater

VariablesStationsGypsumCalcium hypochloriteSodium hypochloriteHydrogen peroxide
Hymenolepis nana (eggs/L) UC 83.74 97.77 85.92 96.26 
CP 89.89 95.61 89.98 97.43 
No 87.85 100 92.8 96.82 
BA 65.50 93.25 85.16 82.35 
Average 81.74 ± 12.88 96.65 ± 9.12 88.46 ± 14.39 93.21 ± 14.55 
Ammonium (mg/L) UC 92.59 94.44 98.21 80.86 
CP 96.29 90.29 95.14 91.71 
No 97.29 91.25 94.79 93.33 
BA 90.21 88.11 93.71 85.31 
Average 94.09 ± 3.28 91.02 ± 2.63 95.46 ± 1.93 87.81 ± 5.78 
Nitrate (mg/L) UC 99.68 99.68 99.99 99.78 
CP 98.51 95.27 97.03 93.11 
No 99.99 99.97 99.98 99.94 
BA 72.73 54.55 99.95 77.27 
Average 92.73 ± 13.35 87.37 ± 21.99 99.24 ± 1.47 92.53 ± 10.65 
Suspended Solids (mg/L) UC 92.07 86.59 82.93 64.02 
CP 98.79 98.44 98.84 98.99 
No 97.79 95.7 88.72 92.79 
BA 74.23 62.69 81.54 61.15 
Average 90.72 ± 11.39 85.85 ± 16.25 88.01 ± 7.87 79.24 ± 19.43 
Turbidity (FTU) UC 92.67 87.53 87.98 88.08 
CP 93.58 94.39 95.97 96.58 
No 99.98 99.99 99.94 99.99 
BA 62.5 53.57 60.71 33.93 
Average 87.18 ± 16.77 83.87 ± 20.83 86.15 ± 17.67 79.65 ± 30.89 
Oxidability (mg/L) UC 99.73 99.73 99.73 99.73 
CP 97.42 91.9 96.01 93.14 
No 99.2 95.71 91.11 91.33 
BA 92.49 95.12 93.39 94.92 
Average 97.21 ± 3.30 95.62 ± 3.21 95.06 ± 3.70 94.78 ± 3.61 
VariablesStationsGypsumCalcium hypochloriteSodium hypochloriteHydrogen peroxide
Hymenolepis nana (eggs/L) UC 83.74 97.77 85.92 96.26 
CP 89.89 95.61 89.98 97.43 
No 87.85 100 92.8 96.82 
BA 65.50 93.25 85.16 82.35 
Average 81.74 ± 12.88 96.65 ± 9.12 88.46 ± 14.39 93.21 ± 14.55 
Ammonium (mg/L) UC 92.59 94.44 98.21 80.86 
CP 96.29 90.29 95.14 91.71 
No 97.29 91.25 94.79 93.33 
BA 90.21 88.11 93.71 85.31 
Average 94.09 ± 3.28 91.02 ± 2.63 95.46 ± 1.93 87.81 ± 5.78 
Nitrate (mg/L) UC 99.68 99.68 99.99 99.78 
CP 98.51 95.27 97.03 93.11 
No 99.99 99.97 99.98 99.94 
BA 72.73 54.55 99.95 77.27 
Average 92.73 ± 13.35 87.37 ± 21.99 99.24 ± 1.47 92.53 ± 10.65 
Suspended Solids (mg/L) UC 92.07 86.59 82.93 64.02 
CP 98.79 98.44 98.84 98.99 
No 97.79 95.7 88.72 92.79 
BA 74.23 62.69 81.54 61.15 
Average 90.72 ± 11.39 85.85 ± 16.25 88.01 ± 7.87 79.24 ± 19.43 
Turbidity (FTU) UC 92.67 87.53 87.98 88.08 
CP 93.58 94.39 95.97 96.58 
No 99.98 99.99 99.94 99.99 
BA 62.5 53.57 60.71 33.93 
Average 87.18 ± 16.77 83.87 ± 20.83 86.15 ± 17.67 79.65 ± 30.89 
Oxidability (mg/L) UC 99.73 99.73 99.73 99.73 
CP 97.42 91.9 96.01 93.14 
No 99.2 95.71 91.11 91.33 
BA 92.49 95.12 93.39 94.92 
Average 97.21 ± 3.30 95.62 ± 3.21 95.06 ± 3.70 94.78 ± 3.61 

UC, University City; CP, Central Prison; No, Nomayos; BA, Biyem-Assi.

Correlation between physico-chemical parameters of the wastewater and viable eggs after disinfection treatment

Significant and positive correlations were recorded at 1% and 5% threshold (Table 2) between some physico-chemical parameters and the number of viable eggs counted. Ammonium (r = 0.95) and nitrates (r = 0.93) were positively and significantly correlated with the viable eggs counted in the control sample. Total suspended solids (TSS) was significantly and positively correlated with viable eggs in the control sample (r = 0.98), and significantly and negatively correlated with gypsum-treated eggs (r = −0.907), and sodium hypochlorite (r = −0.907). Turbidity was significantly and negatively correlated with eggs treated with sodium hypochlorite (r = −0.82). The pH was significantly and negatively correlated with eggs treated with sodium hypochlorite (r = −0.92). The pH was significantly and negatively correlated with eggs treated with calcium hypochlorite (r = −0.92). Nitrates measured after disinfection are positively and significantly correlated with eggs counted in the sample treated with gypsum (r = 0.906), calcium chloride (r = 0.980), sodium hypochlorite (r = 1), hydrogen peroxide (r = 0.959) and control sample (r = 0.984).

Table 2

Table of correlations between physicochemical variables measured before and after disinfection and the number of viable eggs counted in the control and treated samples

V
NOV
NH+3
(mg/L)
NO3
(mg/L)
SS
(mg/L)
Turbidity
(FTU)
pHNO3AD
(mg/L)
Gypsum 0.33 0.31 −0.907* −0.91 0.313 0.906* 
CaCl2 0.47 0.062 −0.348 −0.26 −0.92* 0.980* 
NaClO 0.62 0.016 −0.91* −0.82* 0.235 1.000** 
H2O2 0.93* 0.85 −0.188 −0.1 0.337 0.959* 
Control 0.95* 0.93* 0.987** −0.2 0.285 0.984** 
V
NOV
NH+3
(mg/L)
NO3
(mg/L)
SS
(mg/L)
Turbidity
(FTU)
pHNO3AD
(mg/L)
Gypsum 0.33 0.31 −0.907* −0.91 0.313 0.906* 
CaCl2 0.47 0.062 −0.348 −0.26 −0.92* 0.980* 
NaClO 0.62 0.016 −0.91* −0.82* 0.235 1.000** 
H2O2 0.93* 0.85 −0.188 −0.1 0.337 0.959* 
Control 0.95* 0.93* 0.987** −0.2 0.285 0.984** 

*Significant correlation at 0.05, **Significant correlation at 0.01.

SS, Suspended Solids; NO3, Nitrate; NH+4, Ammonium; NO3−_AD, Nitrate After Disinfection; NOV, Number of Viable Eggs.

Discussion

The presence of Hymenolepis nana eggs in sewage and sewage sludge at high concentrations (636.5 ± 226.81 eggs/L) would be explained by the fact that they are zoonotic parasites. The high densities observed may also be explained by the fact that these are effluents from social housing and prison; therefore the population boom may favour the persistence of this parasite. Indeed, Hymenolepis tends to develop in areas with deficient socio-structural conditions. Promiscuity and contact with populations and rodents would be favourable to the increase of Hymenolepis prevalence because rodents are the main vectors of this zoonosis (Botero & Restrepo 2003; Watwe & Dardi 2008; Fitte et al. 2018). The resurgence of this parasitosis could also be explained by the resistance of this parasite to praziquantel (Beshay 2018).

Calcium chloride makes it possible to render Hymenolepis eggs inactive by degrading their surface lipopolysaccharides. After penetration into the cytoplasm, calcium hypochlorite will react with the DNA by oxidizing the purine bases (adenine and guanine) respectively into 8-chloroadenine and 8-chloroguanine. Sodium hypochlorite enters the cytoplasm through the cell wall and attacks the essential amino acids of the cell. It causes biosynthetic alterations in cell metabolism and destruction of phospholipids. It also attacks the double bonds, leading to the formation of lipids and chlorohydrins (Spickett 2007). These chlorohydrins will have cytotoxic effects and will destabilize the cell membrane by increasing cell polarity (Vissers et al. 2001). Gypsum allows a complexation of microorganisms; thanks to its saline properties, it increases the permeability of the external membrane of eggs (Charpentier et al. 2018). Hydrogen peroxide reacts by inactivating the protein structure and DNA of microorganisms (Halliwel 2006). Once introduced, H2O2 is attracted to the membrane, and then absorbed by the phosphates. This absorption induces an initial disruption of the membrane integrity and consequently, a penetration of the molecule towards the inner membrane, which will bind to the phospholipids. This binding will increase membrane permeability accompanied by the precipitation of cytoplasmic compounds. Similarly, H2O2 leads to a reduction of the egg wall (Ibañez-Cervantes et al. 2013).

Sodium hypochlorite allows us to observe a progressive decrease in the number of viable eggs according to the increase in disinfectant concentration with yields of 85%, 89%, 92%, 85%, respectively, for CU, PC, No and BA stations. Despite the fact that sodium hypochlorite is the most used disinfectant (Ayçiçek et al. 2001; Naidoo et al. 2016), its efficiency does not appear to be real when treating microorganisms in water (Akam et al. 2005; Keffala et al. 2012). Moreover, the uncontrolled use of sodium hypochlorite can lead to the formation of toxic disinfection by-products (Li et al. 2017; Zheng et al. 2017).

The efficacy of gypsum on H. nana eggs does not differ significantly from that of sodium hypochlorite and hydrogen peroxide with yields of 83%, 89%, 87%, 65%, respectively, for CU, PC, No and BA stations. These results may indicate that gypsum can be used as a substitute for conventional disinfectants in water treatment. Contrary to other chemical disinfectants that are synthesized in the laboratory and whose increase in concentration can have harmful effects on organisms, gypsum is a natural product with no known harmful effects on the organism and whose increase in concentration can allow a complete inactivation of microorganisms; moreover, gypsum does not react in solubility with acid and has no radioactive activity (Hennane & Melle 2007). The yields obtained with hydrogen peroxide were 96%, 97%, 96%, 82%, respectively, for CU, PC, No and BA stations. Despite the increase in the concentrations used, hydrogen peroxide did not allow complete inactivation of all Hymenolepis eggs. Akam et al. (2005) observed the ineffectiveness of hydrogen peroxide on Cryptosporidium cysts at (3%).

Among the four disinfectants used, calcium hypochlorite alone showed a 100% performance (Nomayos station) on the inactivation of H. nana eggs. Prolonged exposure of eggs to disinfectants increases their permeability (Clarke & Perry 1998; Johnson et al. 1998). However, at very high concentrations, chlorine has the disadvantage of reacting with organic matter, inducing the formation of chronically toxic organo-halogen compounds (Rook 1974). These two results are similar to those obtained by Bandala et al. (2012) by combining chloride and UV radiation for the disinfection of helminth eggs. The inactivation of Hymenolepis eggs through sodium hypochlorite, hydrogen peroxide and gypsum did not achieve World Health Organization (WHO) guidelines for wastewater reuse (less than one viable egg per litre). However, these disinfection techniques may be used in conjunction with other wastewater treatment processes to achieve this guideline. The high resistance of the H. nana egg could be attributed to the structure of the wall composed of three layers (the capsule, the outer and inner shell) and also to the chemical nature of the egg. Hymenolepis nana eggs are composed of proteins and carbohydrates (mucopolysaccharides), which allows them to remain viable in the environment for long periods (Ibañez-Cervantes et al. 2013).

In addition to the dose of the disinfectant used, physico-chemical parameters are variables to be taken into account when treating water (Plewa et al. 2017; Raquel Chavesa et al. 2019). The toxic by-products formed after disinfection depend on the physico-chemical quality of the water (Li et al. 2017; Zheng et al. 2017).

In general, almost all pH values obtained after treatment with chlorine tend towards basicity, which influences the treatment of helminths (Gaspard & Schwartzbrod 2003). In water, chlorine reacts by establishing an acid/base equilibrium between hypochlorous acid and hypochlorite ion. Hypochlorous acid is the most active chlorine element on microorganisms. This balance is strongly influenced by the pH of the water. The basic pH values obtained will result in a low production of hypochlorous acid. This will negatively influence the inactivation of microorganisms (Rodier 2009). On the other hand, the pH values obtained after treatment with the application of hydrogen peroxide tend towards neutrality, which can influence the effectiveness of hydrogen peroxide; according to Ibañez-Cervantes et al. (2013), hydrogen peroxide is more effective at pH 10. The values of nitrates, ammonium and oxidability obtained on the control samples before disinfection are higher than the standards prescribed by Rodier (2009). After application of disinfectants these values are considerably reduced, but they remain present in all samples. Indeed, ammonia is a parameter to be considered during water treatment (Pecson & Nelson 2005; Fidjeland et al. 2015). The significant and positive correlations observed between ammonia nitrogen, nitrates and viable eggs enumerated in our study illustrate the role played by organic matter during the process of disinfection, as organic matter can adsorb a disinfectant portion and make the amount of disinfectant required to inactivate microorganisms unstable.

The level of suspended solids present in the samples decreased significantly after application of the disinfectants, with reduction rates of 90.72(±11.39)%, 85.85(±16.25)%, 88.01(±7.87)% and 79.24(±19.43)% for gypsum, calcium chloride, sodium hypochlorite and hydrogen peroxide, respectively. Similarly, the turbid matter present in the samples decreased considerably after application of the disinfectant, with reduction rates of 87.18(±16.7)%, 83.87(±20.83)%, 86.15(±17.67)% and 79.65(±30.89)%, respectively, for gypsum, calcium hypochlorite, sodium hypochlorite and hydrogen peroxide.

This study also demonstrated the need to apply a primary treatment when the samples are highly loaded with organic matter, suspended solids and turbidity and to allow a high efficiency of the disinfectants on the targeted microorganisms. The germicidal power of chlorine decreases sharply when the turbidity of the water is greater than 5 FTU. Indeed, during disinfection, the particles present in the water constitute a potential barrier preventing permanent contact between the eggs and the disinfectant (Shimizu et al. 1997; Bougrier et al. 2005). The limited action observed between the various disinfectants used and eggs could be explained by the high turbidity recorded at all stations assessed. The WHO recommends an average turbidity of 1 NTU for water intended for treatment.

The comparison between the disinfectants used and the concentrations shows the significant difference between the control values for all parameters and the values obtained after application of the disinfectants. This suggests that these disinfectants have similar efficiency, and unlike calcium chloride, sodium hypochlorite and hydrogen peroxide, which are chemicals, and therefore their increase in concentration during water treatment may represent a health risk for humans, gypsum is a better alternative because it is a natural product that does not present any toxic effects.

The comparison of the concentrations used shows that the concentrations 0.5 and 0.6 differ significantly from the concentrations 0.1, 0.2, 0.3, 0.4. The maximum activity of the disinfectants on the inactivation of Hymenolepis nana eggs and on the reduction of values of the physico-chemical parameters is felt from concentration 0.5; it would therefore be more judicious to use similar concentrations when treating water.

This study revealed that Hymenolepis nana eggs isolated from the wastewater and sewage sludge are highly resistant to the different disinfectants used for water treatment and their inactivation depends on the physico-chemical nature of the water. Over the four disinfectants assessed, calcium chloride showed a greater efficiency in reducing egg viability with an efficiency rate of 93.12 ± 9.12%, followed by hydrogen peroxide (89.57 ± 14.55%), sodium hypochlorite (82.51 ± 14.39%) and gypsum (80.85 ± 12.88%). The high prevalence of these eggs is linked to some physico-chemical parameters, which favour the survival of these eggs in the environment. The resistance of these eggs to commonly used disinfectants has been demonstrated by the influence of physico-chemical parameters which can inhibit the action of commonly used disinfectants; hence the need to use new and less toxic disinfectants such as gypsum. Gypsum had very significant effects on the inactivation of eggs and could well be used as an alternative for water treatment, as it does not present toxic effects, unlike other chemical disinfectants assessed.

This work was funded by the Laboratory of Hydrobiology and Environment of the University of Yaounde I.

All relevant data are included in the paper or its Supplementary Information.

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