Environ. Sci. Technol. 2009, 43, 6816–6821
Recovery of Biosolids from Constructed Wetlands Used for Faecal Sludge Dewatering in Tropical Regions I V E S M . K E N G N E , †,‡ A M O U G O U A K O A , † ´ * ,‡ AND DOULAYE KONE Laboratory of Environmental Biotechnology, Faculty of Science, University Yaounde´ I, P.O. Box 812, Yaounde´, Cameroon, and Eawag: Swiss Federal Institute of Aquatic Science and Technology, Department of Water and Sanitation ¨ berlandstrasse 133, in Developing Countries (Sandec), U P.O. Box 611, 8600 Du ¨ bendorf, Switzerland
Received November 21, 2008. Revised manuscript received July 4, 2009. Accepted July 15, 2009.
Biosolids recovered from yard-scale vertical-flow constructed wetlands used for fæcal sludge dewatering in Cameroon, were analyzed to assess their degree of maturity, nutrient and heavy metals contents, as well as their hygienic quality. Six beds were loaded weekly at nominal loading rate of 100, 200, and 300 kg TS/m2/year. The quality of the biosolids accumulated in the beds was monitored during 6 additional months of resting period prior to final harvest. Results showed that C/N ratio (11.3), humification index (14%), humification rate (1.8%), and degree of polymerization (3.7) of the biosolids generated were comparable to those of mature composts. Biosolids quality appeared to having high fertilizing value (N: 2%, P2O5: 2.3%, CaO: 1%, MgO: 0.14%, K2O: 0.03, and Na2O: 0.09%) with low heavy metals contamination (63, 14, 26, 2.4, 575, 703, 186, and 32 mg/ kg for Pb, Ni, Cr, Cd, Cu, Zn, Mn, and Se, respectively). The concentration of fertile ascaris was reduced from 40 eggs/g TS after one month storage to 0.05). All the calculations were performed using the statistical software Minitab 14.2 for Windows.
3. Results and Discussion 3.1. Degree of Maturity of Biosolids. The parameters commonly used to characterized compost maturity revealed that the biosolids obtained can be assimilated to mature compost, although the dewatering process was not subjected to the classical mesophilic, thermophilic and maturation phases. Indeed, the C/N ratio of the biosolids obtained was equal to 11, a value close to that generally found in mature composts (Table 2). Furthermore, the humification indices 6818
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parameters pH water pH KCl residual acidity (pH water to pH KCl) conductivity (µS/cm) salinity (‰) CaO (% DM) MgO (% DM) K2O (% DM) Na2O (% DM) total N (% DM) total C (% DM) total P2O5 (% DM) a
no. of samples
mean ( stdev
poultry manurea
18 18
6.01 ( 0.26 5.28 ( 0.22
8.77
18 18 18 24 24 24 24 24 24 12
0.7 ( 0.2 259 ( 112 0.10 ( 0.06 1.04 ( 0.22 0.14 ( 0.04 0.03 ( 0.01 0.09 ( 0.03 2.00 ( 0.20 22.6 ( 3.2 2.3 ( 0.6
3.5 1.75 0.39 0.36 2.4 22.3 2.5
Poultry manure from a farmyard in Yaounde´.
obtained, especially the degree of polymerization, which equals 3.7, was higher than those found in many other mature cocomposts (21, 22). Immature composts generally contain high levels of FA and low levels of HA. During decomposition, the FA fraction either decreases or remains unchanged, while humic acids are produced, leading to a higher degree of polymerization (23). 3.3. pH and Nutrient Content of Biosolids. The biosolids exhibited slightly acidic (pH ≈ 6) to a moderate potential acidity (0.5 < pH water to pH KCl < 1) and presented a low level of salinity (0.1-0.2‰). Their high nutrient contents were similar to those of poultry manure commonly used as organic fertilizer in the region, especially as regards total nitrogen and total phosphorus (Table 3). However, The fertilizing value of the biosolids obtained was slightly less as compared to data reported from similar studies in Bangkok (24) (total organic N, P205, and K2O of 3.0; 2.8, and 0.24%, respectively). Lower nutrient content (0.53 and 1.01% for total organic N and P2O5, respectively) has been reported after cocomposting water lettuce (Pistia stratiotes) with stabilization ponds sludge in Yaounde, Cameroon (25). 3.4. Trace Elements in the Biosolids. Biosolids generated from the constructed wetlands can be recycled in agriculture without fears with respect to heavy metal as they exhibited relative low trace elements concentrations (Table 4). Indeed, concentrations of Pb, Ni, Cr, Cd, Cu, Zn, Mn, and Se were on the order of 63, 14, 26, 2,4, 575, 703, 186, and 32 mg/kg, respectively. These values were even below the limits accepted for sewage sludge in most European countries (26). Concentrations of Pb, Ni, and Cr were even below the limit values of the European Communities eco label composts (Table 4). These results showed that the mechanically emptied fæcal sludge from this city is not highly contaminated by heavy metals, thus increasing the potential for valorisation of biosolids produced by the FS treatment plant. 3.5. Hygienic Quality of the Biosolids. 3.5.1. Occurrence of Helminth Eggs in Biosolids Stored for One Month. 3.5.1.1. Overall Occurrence. Biosolids removed one month after stopping sludge applications revealed high concentration of helminth eggs. Globally, almost all the helminth eggs belong to the Nematoda class (Ascaris, Trichuris, Ancylostoma, Enterobius, Strongyloides stercoralis) (Table 5). Ascaris lumbricoides was the most widespread helminth specie found (73% of the total counts), followed by Trichuris trichiura (25%), Strongyloides stercoralis (0.7%), Ancylostoma duodenale, and Enterobius vermicularis (0.6% each). Taenia sp. (Cestoda) was found in only one count, thus representing 0.1% of the total count. The concentration of Ascaris eggs in the biosolids remained high as in the raw sludge. This nematode species has an extremely high prevalence in
TABLE 4. Trace Elements in Biosolids Recovered from the Constructed Wetlands trace elements concentration (mg/kg)
parameters
biosolids
Fe Pb Ni Cr Cd Cu Zn Mn Se Si
9579 ( 14 63 ( 32 14 ( 3 26 ( 4 2,4 ( 0,8 575 ( 283 703 ( 436 186 ( 25 32 ( 16 2779 ( 551
limit values in EC eco label compost (Hogg et al., 2002)
limit values in Spain sewage sludge (Hogg et al., 2002)
100 50 100 1 100 50
750 300 1000 20 1000 2500
FIGURE 1. Distribution of helminth eggs and dry matter content in biosolids as a function of storage time.
TABLE 5. Helminth Eggs Species Isolated in the FS Biosolids after One Month of Storage (n = 54) helminth species (count/g TS) Ascaris lumbricoides fertile Ascaris lumbricoides infertile Trichirus trichuira Ancylostoma duodenale Strongyloides stercoralis Enterobius vermicularis Tenia sp. Total eggs
mean median stdev maximum 38.5 19.4 19.5 0.5 0.6 0.5 0.9 78.9
23.4 13.3 9.8 0 0 0 0 56.3
42.1 18.1 26.4 1.5 1.7 1.0 0.7 65.7
172 72 146.7 8 8.9 4 5.3 305.3
developing countries (6). On average, approximately 79 helminth eggs (total counts) were obtained per g TS in the drying beds. This number was relatively higher than the 22-38 eggs/g TS reported in dewatered biosolids in Ghana (27). The fertile form of A. lumbricoides was most widespread, with almost 67% of the total count (Table 5). Kone´ et al. (27) reported a viability of 25-50% of Ascaris and Trichuris eggs in dewatered fæcal sludge from unplanted drying beds in Kumasi (Ghana). Therefore, the biosolids removed from beds at after one month storage could not be used or recommended for agricultural purpose as the probability to have infective form could be higher. 3.5.1.2. Distribution of Helminth Eggs in Sludge Layers. Results of helminth eggs analysis in sludge stored for one month revealed a decrease in concentration with respect to depth: the upper part of the sludge containing almost 54% of the total egg counts and only 14% at the bottom of the beds (Table 6). This may be attributed to the fact that the upper biosolids layer was formed by freshly deposited raw FS, whereas the sludge present at the bottom was more stabilized, thus leading to the destruction of eggs during storage. Indeed, storage time has been found to contribute to weakening the external membranes of the eggs, which may be degraded by bacteria and fungi present in the biosolids (28).
3.5.2. Evolution of Helminth Eggs As a Function of Time. As expected, a significant egg reduction (90%) in the biosolids was noted with increasing storage time. Indeed, the average eggs total count decreased from 78.9 to 7.5 eggs/g TS after six months of storage (Figure 1). No Ancylostoma duodenale, Strongyloides stercoralis, Enterobius vermicularis, and Tenia sp. eggs were determined after four months. Fertile Ascaris eggs also decreased from 38.5 after one month to only 4.03 eggs/g TS after six months, resulting in a reduction of almost 89%. This significant decrease in helminth eggs may be attributed to bacteria decomposition (29), attack by nematophagous fungi (30, 31) as well as adverse environmental conditions, especially the reduction of moisture content of biosolids. Indeed, a reduction in moisture content was observed, with an average dry matter increasing from 51% one month after storage to 77% six months later (Figure 1). These findings corroborate those of Sanguinetti et al. (28), who found a significant reduction of Ascaris viability with decreasing humidity under dry bed conditions in Argentina. Although the temperature was not measured in the accumulated layer of biosolids, this parameter could not be considered as a key factor influencing Ascaris eggs inactivation in this study. Indeed, according to Embrechts and Tavernier (8), an average air temperature ranging from 18 to 30 °C, as observed in Yaounde, will increased soil temperature to maximum 2.3-2.6 °C. Hence, the maximum temperature in the biosolids was considered to be less than the lethal level of 40-45 °C described in the literature (32). Biological stressors such as organic acids, aldehydes, and alcohols have been shown to act as disinfectants of pathogens in biosolids (33). Despite this reduction, the biosolids may not be entirely sanitized after this storage period as regards compliance with the WHO established standards of less than 1 egg/g TS for safe agricultural practice (6), since we only investigated Ascaris eggs’ fertility. Hence prior to direct application on field, further storage for at least one month protected from rain or an additional treatment by ammonia, urea may be recommended (34). Cocomposting
TABLE 6. Distribution of Helminth Eggs As a Function of Depth One Month after Loading Was Stoppeda no. of helminth eggs/g TS depth
no. of samples
DM (%)
fertile asc.
infertile asc.
tric.
anc.
stro.
ent.
tae.
total eggs
upper surface (5 cm) centre bottom (last 5 cm)
18 18 18
45.3 49.1 58.8
65.5 36.5 13.4
27.3 20.2 10.6
32.6 17.6 8.3
0.7 0.4 0.3
0.9 0.6 0
0.4 0.4 0.6
0 0 0.3
127.4a 75.8b 34c
a Row values followed by the same letter are not statistically significant (p > 0.05). Asc.: Ascaris lumbricoides; Tric.: Trichuris trichiura; Anc.: Ancylostoma duodenale; Ent.: Enterobius vermicularis; Tae.: Taenia sp.
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has been suggested and tested successfully as a mean to rapidly sanitized sewage biosolids, since the higher temperatures of the thermophilic phase have been observed to significantly affect the inactivation rate of pathogens (27). Our findings nevertheless confirmed the beneficial effects of longer storage periods on parasite reduction. From this study, it can be concluded that a minimum of six month storage time is required to sanitize fæcal sludge on planted dewatering beds under tropical conditions. Based on epidemiological and the quantitative microbial risk assessment (QMRA), Navarro et al. (35) showed that higher helminth eggs concentration in biosolids did not significantly increase consumers and famers health risk exposure. Indeed, the current WHO guidelines (6) were not developed using an epidemiological approach. As a consequence, the indicative standard of 1 helminth egg/g TS in biosolids appears to be more stringent and unaffordable in most cases in developing countries. Studies on the commercialization of these biosolids could help generate substantial funds to run the VFCW plant, therefore linking sanitation management and urban food production systems in developing countries.
Acknowledgments We acknowledge the support provided by the Swiss National Centre of Competence in Research (NCCR) North-South: Research Partnerships for Mitigating Syndromes of Global Change, cofunded by the Swiss National Science Foundation (SNF) and the Swiss Agency for Development and Cooperation (SDC). It also benefited the support of the International Foundation for Science (IFS, Sweden, grant W4115/1). We express our special thanks to Rose Ndango (International Institute for Tropical Agriculture, Cameroon), Henriette Ndam (Institute of Agricultural Research for Development (IRAD, Cameroon), Claudia Baenninger (Swiss Federal Institute of Aquatic Science and Technology), and Rachelle Ganwa for their assistance in sample analyses.
Literature Cited (1) von Braun, J.; Fan, S.; Meinzen-Dick, R.; Rosegrant, M. W.; Pratt, A. N., International Agricultural Research for Food Security, Poverty Reduction, and the Environment - What to Expect from Scaling Up CGIAR Investments and “Best Bet” Programs; International Food Policy Research Institute:, Washington, DC, 2008. (2) Vinnerås, B. Comparison of composting, storage and urea treatment for sanitising of faecal matter and manure. Bioresour. Technol. 2007, 98 (17), 3317–3321. (3) Chin, Y.-P.; Weber, W. J. J. Estimating the effect of dispersed organic polymers on the sorption of contaminants by natural solids. 1. A predictive thermodynamic humic substance-organic solute interaction model. Environ. Sci. Technol. 1989, 23 (8), 978–984. (4) Scott, D.; McKnight, D.; Blunt-Harris, E.; Kolesar, S.; Lovley, D. Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ. Sci. Technol. 1998, 32 (19), 2984–2989. (5) Lienert, J.; Gudel, K.; Escher, B. I. Screening method for ecotoxicological hazard assessment of 42 pharmaceuticals considering human metabolism and excretory routes. Environ. Sci. Technol. 2007, 41 (12), 4471–4478. (6) WHO, Guidelines for the Safe Use of Wastewater, Excreta and Greywater; World Health Organization: Geneva 2006; Vol. 4, p 182. (7) Kengne, I. M.; Akoa, A.; Soh, E. K.; Tsama, V.; Ngoutane, M. M.; Dodane, P. H.; Kone´, D. Effects of faecal sludge application on growth characteristics and chemical composition of Echinochloa pyramidalis (Lam.) Hitch. and Chase and Cyperus papyrus L. Ecol. Eng. 2008, 34 (3), 233–242. (8) Embrechts, J.; Tavernier, R. Soil temperature regimes in cameroon as defined in soil taxonomy. Geoderma 1986, 37, 149–155. (9) Anderson, D. W.; Schoenau, J. J., Soil Humus fractions. In Soil Sampling and Methods of Analysis; Carter, M. R., Ed.; Lewis Publishers: Boca Raton, FL, 1993; Vol. 38, pp 391-395. 6820
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 17, 2009
(10) Tiessen, H.; Moir, J. O., Total and organic carbon. In Soil Sampling and Methods of Analysis; Carter, M. R., Ed.; Lewis Publishers: Boca Raton, FL, 1993; pp 187-199. (11) Sanchez-Monedero, M. A.; Roig, A.; Cegarra, J.; Bernal, M. P. Relationships between water-soluble carbohydrate and phenol fractions and the humification indices of different organic wastes during composting. Bioresour. Technol. 1999, 70 (2), 193–201. (12) Soltner, D. Les Bases De La Production Ve´ge´tale, 9th ed.;Sciences et Techniques Agricoles: Sainte-Gemmes-sur-Loire, 1980; p 455. (13) Eaton, A. D.; Franson, M. A. H., Standard Methods for the Examination of Water and Wastewater, 21st ed.; American Public Health Association: Washington, DC, 2005; p 1368. (14) Heanes, D. L. Determination of organic Carbon in soils by an improved chronic acid digestion and spectrophotometric procedure. Soil Sci. Plant Anal. 1984, 15, 1191–1213. (15) Buondono, A.; Rashad, A. A.; Coppola, E. Comparing tests for soil fertility. 11. The hydrogen peroxide/sulfiric acid treatment as an alternative to copper/selenium catalyzed digestion process for routine determination of soil nitrogen-Kjedahl. Soil Sci. Plant Anal. 1995, 26, 1607–1619. (16) Anderson, J. M. Tropical Soil Biology and Fertility: A Handbook of Methods, 2nd ed.; CAB International: Wallingford, 1993; Vol XV, p 221. (17) Mehlich, M. Mehlich 3 soil test extractant: a modification of the Mehlich 2 extractant. Soil. Sci. Plant Anal. 1984, 15, 1409–1416. (18) Murphy, J.; Riley, J. P. A modified single solution method for determination of phosphate in natural waters. Anal. Chim. Acta 1962, 27, 31–36. (19) Schwartzbrod, J. Methods of Analysis of Helminth Eggs and Cysts in Wastewater, Sludge, Soil and Crops. In University of Nancy: 2003; p 12. (20) WHO. Bench Aids for the Diagnosis of Intestinal Parasites, NLM classification: WC 698; WHO: Geneva, 2003. (21) Aparna, C.; Saritha, P.; Himabindu, V.; Anjaneyulu, Y. Techniques for the evaluation of maturity for composts of industrially contaminated lake sediments. Waste Manage. 2008, 28 (10), 1773–1784. (22) Jouraiphy, A.; Amir, S.; El Gharous, M.; Revel, J.-C.; Hafidi, M. Chemical and spectroscopic analysis of organic matter transformation during composting of sewage sludge and green plant waste. Int. Biodeterior. Biodegrad. 2005, 56 (2), 101–108. (23) Tuomela, M.; Vikman, M.; Hatakka, A.; Itavaara, M. Biodegradation of lignin in a compost environment:A review. Bioresour. Technol. 2000, 72 (2), 169–183. (24) Kost, M.; Marty, P. Septage Treatment by Constructed Wetlands, Report on practical training; AIT/SANDEC, 2000, p 43. (25) Agendia, P. L.; Kengne Noumsi, I. M.; Fonkou, T.; Mefenya, R.; Sonwa, D. J. Production de compost a` partir de la biomasse de Pistia stratiotes. Cah. Agric. 1997, 6, 15–9. (26) Hogg, D.; Barth, J.; Favoino, E.; Centemero, M.; Caimi, V.; Amlinger, F.; Devliegher, W.; Brinton, W.; Antler, S. Comparison of Compost Standards within the EU, North America and Australasia; The Waste and Resources Action Programme: Oxon, UK, 2002; pp 1-97. (27) Kone´, D.; Cofie, O.; Zurbrugg, C.; Gallizzi, K.; Moser, D.; Drescher, S.; Strauss, M. Helminth eggs inactivation efficiency by faecal sludge dewatering and co-composting in tropical climates. Water Res. 2007, 41 (19), 4397–4402. (28) Sanguinetti, G. S.; Tortul, C.; Garcia, M. C.; Ferrer, V.; Montangero, A.; Strauss, M. Investigating helminth eggs and Salmonella sp. in stabilization ponds treating septage. Water Sci. Technol. 2005, 51 (12), 239–247. (29) Akhtar, M.; Malik, A. Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresour. Technol. 2000, 74 (1), 35–47. (30) Ahman, J.; Johansson, T.; Olsson, M.; Punt, P. J.; van den Hondel, C. A. M. J. J.; Tunlid, A. Improving the pathogenicity of a nematode-trapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Appl. Environ. Microbiol. 2002, 68 (7), 3408–3415. (31) Brian R. Kerry, J. M. B. The importance of rhizosphere interactions in the biological control of plant parasitic nematodes - A case study using Verticillium chlamydosporium. Pestic. Sci. 1996, 47 (1), 69–75. (32) Feachem, R. G.; Bradley, D. J.; Garelick, H.; Mara, D. D., Sanitation and Disease Health Aspects of Excreta and Wastewater Management; Wiley: Chichester a.o., 1983; Vol. XXVII, 501. (33) Smith, J. E. J.; Surampalli, R. Y.; Reimers, R. S.; Tyagi, R. D.; Lohani, B. N. Disinfection processes and stability refinements to biosolids treatment technologies. Pract. Period. Hazard., Toxic, and Radioact. Waste Manage. 2008, 12 (1), 10–17.
(34) Pecson, B. M.; Barrios, J. A.; Jime´nez, B. E.; Nelson, K. L. The effects of temperature, pH, and ammonia concentration on the inactivation of Ascaris eggs in sewage sludge. Water Res. 2007, 41 (13), 2893–2902. (35) Navarro, I.; Jime´nez, B.; Cifuentes, E.; Lucario, S. In A Quantitative Microbial Risk Assessment of Helminth Ova in Reusing Sludge
for Agricultural Production in Developing Countries, Risk Analysis VI, WIT Transactions on Information and Communication; Beriatos, C. A. B. a. E., Ed.; WIT Press, University of Thessaly: Greece, 2008; p 576.
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