Hygienic quality of faeces treated in urine diverting vermicomposting toilets

Waste Management 33 (2013) 2204–2210

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Hygienic quality of faeces treated in urine diverting vermicomposting toilets Cecilia H. Lalander a,⇑, Geoffrey B. Hill b, Björn Vinnerås a,c a

Department of Energy and Technology, Swedish University of Agricultural Sciences, Uppsala, Sweden University of British Columbia, Vancouver, Canada c National Veterinary Institute, Uppsala, Sweden b

a r t i c l e

i n f o

Article history: Received 14 May 2013 Accepted 1 July 2013 Available online 6 August 2013 Keywords: Fertiliser Hygiene On-site sanitation Sanitisation Urine diverting toilet Vermicomposting

a b s t r a c t On-site sanitation solutions have gained much interest in recent years. One such solution is the urine diverting vermicomposting toilet (UDVT). This study evaluated the hygienic quality of the composted material in six UDVTs in operation in France. Samples were taken from three sampling positions in each toilet, with increasing distance from the fresh material. The concentration of Salmonella spp., Enterococcus spp., thermotolarent coliforms and coliphages were analysed and plotted against a number of variables. The variables found to have the greatest impact was the pH (for Enterococcus spp. and thermotolarent coliforms (TTC)) and time since last maintenance (coliphages). The pH was found to correlate with the material maturity. The current practise of maintenance can cause recontamination of the stabilised material and increase the risk of regrowth of pathogenic microorganisms. A modification in the maintenance procedure, in which a fourth maturation point is introduced, would eliminate this risk. UDVTs were found to be a good on-site sanitation option as the maintenance requirement is small and the system effectively reduced odour and concentration of pathogen and indicator organisms in human waste while keeping the accumulation of material down to a minimum. If the vermicompost is to be used for crops consumed raw, an additional sanitisation step is recommended. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction Sanitation is defined as the collection and treatment of human excreta to ensure the well-being of the individuals of a community (Group, 1987). The coverage of improved sanitation is high in highincome countries; toilet wastewater is treated centrally at treatment plants, so-called off-site sanitation, run by the municipality. In remote areas and in summer cottages the coverage of municipal sanitation is not as complete and on-site sanitation solutions are often practised (Lebersorger et al., 2011). The situation worldwide is very different: 1.2 billion people lack access to sanitation, the vast majority of these people live in low- and middle-income countries (UNICEF/WHO, 2012). The development of improved sanitation in these areas will most likely be on-site decentralised sanitation solutions and not the centralised solutions that have dominated the development in sanitation technology in high-income countries for half a century (Massoud et al., 2009). On-site sanitation systems can be very simple or more technologically complex (Franceys et al., 1992). Commonly available on-site sanitation systems today are composting latrines and urine diverting dry toilets (UUDT). The treatment of the collected fraction vary with system, it can be ⇑ Corresponding author. E-mail address: [email protected] (C.H. Lalander). 0956-053X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.wasman.2013.07.007

composted, stored, burned or treated in a small treatment plant (Strauss et al., 1997; Kavanagh, 2005). In some of these systems the collected fraction is viewed as waste that has to be collected in order to prevent environmental pollution and ensure the health of the community (Cilimburg et al., 2000), while it in other systems is viewed as a resource that can be used for food production if handled appropriately (Jönsson et al., 2008). One way of treating the solid fraction from UDDTs (faeces and toilet paper) is by composting. The composting can be accelerated by the action of worms. Epigeic earthworms facilitates microbial decomposition by fragmenting the waste mechanically, maintaining aerobic conditions and changing the biochemical properties of the material (Loehr et al., 1985). The final material is highly porous with greatly improved water holding capacities and nutrients in forms readily available to plants (Dominguez, 2010). The most commonly used earthworm species in vermicomposting are Eisenia foetida, Eisenia andrei and Dendrobaena veneta, used because of their short life cycles, high reproduction rate, tolerance to a wide range of temperatures and endurance of handling (Dominguez and Edwards, 2010). In a vermicomposting toilet, the urine has to be diverted as the worms are highly sensitive to ammonia and inorganic salts (Dominguez and Edwards, 2011), thus the system can be defined as a urine diverting vermicomposting toilet (UDVT).

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The vermicomposting technology has been explored on a wide variety of organic wastes, including sewage sludge, municipal waste, pig and cow manure and human excrement (Dominguez et al., 2000; Aalok et al., 2008; Aira et al., 2002; Contreras-Ramos et al., 2005; Yadav et al., 2010). Buzie-Fru (2010) demonstrated the feasibility of using the vermicomposting technology as treatment of source separated faeces. In his thesis he developed and tested a continuous single chamber vermicomposting toilet. He found that optimal conditions for vermicomposting of faeces was at a moisture content of 65–80% at 20–25 °C, achieving 50–80% reduction in organic carbon after 96 days of treatment. The main question with UDVTs is whether the processed material, aside from being stabilised, also can be considered hygienically safe. Numerous reports demonstrate the capacity of vermicomposting systems to inactivate Enterobacteriaceae, such as Salmonella spp., Escherichia coli and Shigella spp. (Contreras-Ramos et al., 2005; Monroy et al., 2009; Kumar and Shweta, 2011). However, opinions differ whether vermicomposting has the ability to destroy or inactivate parasites such as the intestinal worm Ascaris spp. (Eastman et al., 2001; Bowman et al., 2006; Hill et al., 2013), while little is known about its effect on viruses. In this study, the hygienic quality of human waste treated in UDVTs – employing epigeic earthworm Eisenia foetida – that had been in operation between two and five years, was investigated. The concentrations of Salmonella spp., Enterococcus spp., thermotolarent coliforms and naturally occurring coliphages (used as indicator for animal viruses), as well as physico-chemical parameters, were analysed.

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necessary. Roughly estimated, around 100–200 kg is relocated from pos 1 to pos 3 at maintenance, which occurs once or twice yearly, although less frequent maintenance occur at toilets with lower yearly number of users (once every two years). The worms present at pos 3 consume the organic material and thereby accelerate the decomposition. Pos 2 is the position between the drop point and the vermicompost and was selected in order to investigate whether a gradient in the concentration of pathogens and indicator organisms could be established. 2.2. Sampling sites Six vermicomposting toilets, in operation between two and six years, were sampled. The different toilets were named site 1–6. The toilets were situated at altitudes between 200 and 2000 m above mean sea level (AMSL). Time since last maintenance (TSLM) varied between 100 and 720 days. Details of the sampled toilets are available in Supplementary material. 2.3. Sampling Three random grab samples were collected from each position (1, 2 and 3), in total 9 samples per toilet. The material was collected in 50 mL centrifuge tubes (approximately 20–30 g per sample) and kept in a cooler until analysis, which occurred within a week of sampling. One replicate per sample was analysed for each parameter.

2. Materials and methods

2.4. Microbial analysis

2.1. UDVT system set-up

One gram of material was dispersed into 9 mL buffered 0.9% NaCl peptone water with 0.1% surfactant Tween 80 (pH 7) and further diluted to 105 of original concentration in the same buffer.

A schematic representation of the UDVT systems evaluated in this study is displayed in Fig. 1. The urine is diverted and infiltrated in the ground. The faeces and toilet paper land on a pedal operated conveyour belt and is transported to a back chamber where it is dropped and accumulated at the drop point (pos 1, Fig. 1). Approximately 1 m from the drop point (centre to centre), a bed of straw is laid (pos 3, Fig. 1; 1  1 m), into which around 2000 earthworms of species Eisenia foetida are placed at the time of installation. The installed earthworms, as well as the ones naturally present on the outside, can move freely in and out of pos 3. The number of worms is thus not constant but depend on the amount of material and condition (temperature, moisture level, pH, NH3 concentration etc.) at pos 3. When necessary the material accumulated at the drop point is manually moved onto pos 3. The relocation of material from pos 1 to pos 3 is referred to as maintenance. The frequency of maintenance is not regulated but occur when the operator deem

2.4.1. Salmonella spp. The concentration of Salm. spp. was determined by most probable number (MPN) method using a three tube set-up. For the preenrichment, one gram of material was dispersed into 9 mL buffered peptone water and incubated at 37 °C for 17–18 h. Three plates of the selective medium Semisolid Rappaport–Vassiliadis (MSRV) were used for each dilution for the MPN analysis. Three drops of the pre-enrichment solution were inoculated onto the MSRV plate using a 10 lL inoculation loop. The plates were inoculated at 41.5 °C for 17 h. A grey-white, turbid zone around the drops indicate positive results. Positive results were confirmed with xylose lysine desoxycholate agar (XLD) plates (Oxoid AB, Sweden) containing 0.15% sodium-novobiocin. XLD plates were incubated at 37 °C for 24 h.

Fig. 1. Schematic representation of the set-up of the vermicomposting toilet treatment chamber, with sample position 1, 2 and 3 depicted (not to scale).

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2.4.2. Thermotolarent coliforms Total thermotolarent coliforms (TTC) were enumerated in double layer agar using violet red bile agar (VRB) (Oxoid AB, Sweden); 1 mL of sample was mixed with 7–8 mL of agar and upon solidification of the first layer, additional 7–8 mL agar was added. The plates were incubated at 44 °C for 24 h. 2.4.3. Enterococcus spp. The concentration of Ent. spp. was decided using a three tube MPN set-up. The selective broth Enterococcosel was used for cultivation; 200 lL sample was immersed into 2 mL broth and incubated at 37 °C for 17–20 h. A colour change to black is indicative of growth of Ent. spp. and were counted as positive. 2.4.4. Coliphages The host of bacteriophage UX174, Escherichia coli (ATCC 13706), was used as host for naturally occurring coliphages and was cultivated in unselective microbial medium (NB, Oxoid AB, Sweden) at 37 °C for 4–12 h. One mL of sample of suitable dilutions was mixed with 2 mL soft agar and 1 mL host solution and poured onto blood agar base (BAB) plates (Oxoid AB, Sweden). The plates were incubated at 37 °C for 17 ± 2 h.

was diluted in 25 mL deionised water and was left to settle for 1 h at room temperature prior to analysis. 2.5.3. Uncharged ammonia One gram of material was diluted nine (pos 1) or four (pos 2–3) times in deionised water. The solution was filtered through a membrane filter (0.45 lm) and stored at 4 °C until analysis (within two days). The concentration of total ammonium nitrogen (TAN) in the filtered solutions was measured photometrically using ammonium test from Merck (kit number 1.00683.0001). The concentration of uncharged ammonia was calculated using the dissociation constant pKa ¼ 0:09018 þ 2729:92 (Clement and Merlin, 1995). T 2.5.4. SolvitaÒ compost maturity The three grab samples from each level were pooled and the compost maturity of the pooled sample evaluated. SolvitaÒ compost maturity test was conducted following instructions provided by the manufacturer. 2.6. Statistical analysis The generalised linear model was used for regression analysis. All analyses and graphical presentations were conducted in R (R Development Core Team, 2011).

2.5. Physico-chemical analysis 2.5.1. Total solids and total volatile solids The material was dried at 105 °C for 14 h for determination of total solids (TS) and at 550 °C for 6 h for determination of total volatile solids (VS). 2.5.2. pH A radiometer electrode was used to measure pH. All analyses were conducted at room temperature (RT). Five gram of sample

3. Results and discussion 3.1. Conditions at pos 1, pos 2 and pos 3 The concentrations of the analysed parameters at the three sampling positions were averaged for the six toilets (Table 1). When comparing the concentrations of the analysed parameters at pos 1 and pos 3 (excluding pos 2) there was a significant reduction in VS and in the concentration of NH3, Salm. spp., TTC, Ent. spp., and

Table 1 The average concentration (SD) in sampling position 1, 2 and 3 of TS (%), VS (%), pH, NH3 (mg kg1 TS), TTC (log10 CFU g1), Ent. spp. (log10 MPN g1), Salm. spp. (MNP g1) and Coliphages (log10 PFU g1). VS (%)

pH

NH3 (mg kg1 TS)

TTC (log10 CFU g1)a

Ent. spp. (log10 MPN g1)a

Salm. spp. (MPN g1)

Coliphages (log10 PFU g1)a

1 2 3

24.5(8.5) 29.7(10.5) 26.6(14.7)

73.7(16.9) 63.2(17.0) 62.7(6.0)

7.4(0.6) 7.1(0.4) 7.3(0.4)

44.7(57.4) 8.4(13.1) 2.9(2.6)

4.98(1.17) 3.94(1.68) 3.06(1.24)

5.66(0.89) 5.27(1.00) 4.14(1.45)

0.15(0.21) 0.14(0.09)

3.18(0.66) 3.15(1.59) 1.70(1.81)

b

Given in log10 concentration. To get the concentration in general number form, the value displayed in the table (e.g. 5) is taken to the power of 10 (i.e. 105 = 100,000). Below the detection limit (0.1 MPN g1).

Log10 concentration (CFU g−1)

b

TS (%)

7 6 5 4 3 2 1

R2 = 0.25 p = 0.035

0 0

200

400

600

800

Log10 concentration (CFU g−1)

a

POS

4 3 2 1 0

R2 = 0.648 p = 5.6 × 10−5

6.6

6.8

7.0

7.2

7.4

pH

Fig. 2. Log10 concentrations of Ent. spp. (MPN g1) in pos 3 at the different sites, plotted against the (a) TSLM and (b) pH; R2; p and 95% confidence interval levels displayed in graphs.

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coliphages (Table 1). When including pos 2 in the regression, the variation within each toilet was too large and no significant trend was established. When analysing the concentration of the studied microorganisms for each toilet separately the trend of reduction from pos 1 to pos 3 (including pos 2) was significant in many, but not all, toilets. Additional factors, apart from the distance from drop-point, appeared to have an impact on the concentration of microorganisms. In order to better understand the factors influencing the hygienic quality of the material in these systems, a more thorough data analysis was made on the conditions influencing the concentration of studied microorganisms at pos 3, the vermicomposting bed. Although Salm. spp. was detected at some sites in pos 1 and 2, no was found in pos 3 (detection limit 0.1 MPN g1) at any site. This is in accordance with previous findings that Salm. spp. is removed during vermicomposting (Contreras-Ramos et al., 2005; Kumar and Shweta, 2011). Salmonella is a zoonotic bacteria of major concern in agriculture as it infects humans, cattle, horses, birds and pigs and can survive for a long time in the soil (Jamieson et al., 2002).

extend, although the R2 was quite low, and with the pH to a greater extend (Fig. 2b). The concentration of TTC did not correlate with the TSLM (Fig. 3a), nor was the correlation with the pH very strong (R2 < 0.5) although it was statistically significant (p < 0.05) (Fig. 3b). The concentration of coliphages was found to correlate with TSLM (Fig. 4a), but not with the pH (Fig. 4b). When plotting the physico-chemical parameters against the TSLM it was found that pH (Fig. 5a) and percentage TS (Fig. 5c) decreased and increased, respectively, with TSLM, while the concentration of NH3 (Fig. 5b) and percentage VS (Fig. 5d) did not correlate. The TS increased from 20% after 100 days of uninterrupted vermicomposting to around 40–60% after 720 days without maintenance. At the toilet with the lowest moisture content only few worms were found. In most toilets the TS was 20%, i.e. an optimal moisture content for vermicomposting.

3.3. Compost maturity at pos 3

Log10 concentration (CFU g−1)

The concentration of Ent. spp., TTC and coliphages at pos 3 were plotted against a number of factors: pH, NH3, TS, VS, TSLM and SolvitaÒ maturity index. The factors demonstrated to have the greatest impact was pH and TSLM. The concentration of Ent. spp. was demonstrated to be correlate with the TSLM (Fig. 2a) to some

5 4 3 2 1 R2 = 0.085 p = 0.256

0 0

200

400

600

The vermicompost (pos 3) was laid on a bed of straw. The straw added extra carbon to pos 3 making it difficult to correlate de degradation of material with the percentage VS (Fig. 5d). Another measure of maturity is the SolvitaÒ maturity index, determined by a combined measure of the concentrations of uncharged NH3 (from 1 high to 5 low) and CO2 (from 1 high to 8 low) in the compost, yielding a rating of stability/maturity that ranges from 1 (active,

Log10 concentration (CFU g−1)

3.2. Effect of TSLM and pH on measured parameters

5 4 3 2 1 0 −1 −2

R2 = 0.321 p = 0.018

6.6

800

6.8

7.0

7.2

7.4

pH

6

Log10 concentration (PFU g−1)

Log10 concentration (PFU g−1)

Fig. 3. Log10 concentrations of TTC (CFU g1) in pos 3 at the different sites, plotted against the (a) TSLM and (b) pH; R2, p and 95% confidence interval levels displayed in graphs.

4

2

0 R2 = 0.572 p = 3 × 10−4

−2 0

200

400

600

800

5

R2 = 0.194 p = 0.068

4 3 2 1 0 6.6

6.8

7.0

7.2

7.4

pH

Fig. 4. Log10 concentrations of coliphages (PFU g1) in pos 3 at the different sites, plotted against the (a) TSLM and (b) pH; R2, p and 95% confidence interval levels displayed in graphs.

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‘‘raw’’ compost) to 8 (inactive, ‘‘finished’’ compost). The concentration of uncharged ammonia gives an indication of the maturity and age of the material, while the CO2 concentration gives an indication of stability of the material based on microbial activity, where low activity indicates stable compost. Hill et al. (2013) suggested the use of SolvitaÒ NH3 index to verify the concentration of uncharged NH3 in latrines, to establish whether the latrine material could be vermicomposted, as earthworms are sensitive to high ammonia concentrations (Dominguez, 2010), which can be a problem when composting fresh human faeces (Yadav et al., 2010). A SolvitaÒ maturity index of 1 would be lethal to the worms, while an index of 5 would pose no risk. The SolvitaÒ test was conducted at all sites at pos 3, except site 2 (Table 2). At all locations the SolvitaÒ NH3 index was 5, while the CO2 index indicated that the activity at site 6 (the most elevated site) was still high. No correlation between the concentration of microorganisms and the SolvitaÒ maturity index was found (p > 0.05). When plotting the maturity index against the pH a significant correlation was seen (Fig. 6), with higher pH correlating with lower maturity index. As the material from each sampling position was pooled into one maturity test, variations within pos 3 are not accounted for and consequently the R2 value is low. A reduction in pH have been demonstrated to correlate with maturity in vermicomposting systems (Ndegwa et al., 2000; Buzie-Fru, 2010). Several explanations to this phenomena exist, among others the mineralisation of nitrogen compounds followed by nitrification (Ndegwa et al., 2000) and the production of carbon dioxide and organic acids as a consequence of the degradation of organic material (Elvira et al., 1998). The pH decreased with TSLM, from around 8 after 100 days since TSLM to 6.5  7 after 750 days

Table 2 SolvitaÒ maturity index for sampling pos 3 at the different sites. Site

NH4-index

CO2-index

Maturity index

1 3 4 5 6

5 5 5 5 5

6 8 7 6 4

6 8 7 6 4

of uninterrupted vermicomposting (Fig. 5a). Although the pH is substrate dependent, the substrate in the different toilets can be assumed to be more or less the same (faeces and toilet paper). When plotting the concentrations of microorganisms to pH it was found to correlate well with the concentration of Ent. spp. but only weakly with the concentration of TTC, while no correlation was found with the concentration of coliphages. The pH was measured for each sample, as opposed to the TSLM, which was the same for the entire site, and could thus better display variations of maturity within pos 3. As the concentration of bacteria correlated better with the pH than the TSLM, the reduction of bacteria appeared to correlated with the material maturity, while the coliphage concentration did not. Not much information can be found about the reduction of viruses and bacteriophages in vermicomposting systems. In a study concerning another biological system, i.e. black solider fly composting, it was found that the reduction of bacteriophage UX174 decreased equally much in the control as in the larval treatment and was thus likely caused by natural, time dependent, degradation and unaffected by the passage through the digestive system of invertebrates (Lalander et al., 2013). It does not

8.0

pH

7.5

7.0

6.5 R2 = 0.786 p = 10 × 10−7

6.0 0

200

400

100

600

Concentration (mg kg−1 TS)

12 10 8 6 4 2 0

800

R2 = 0.615 p = 5 × 10−4

0

200

400

100

80

80

60

60

40

40

20

20

0

R2 = 0.131 p = 0.248

600

800

R2 = 0.211 p = 0.654

0 0

200

400

600

800

0

200

400

600

800

Fig. 5. Physico-chemical parameters of the material in pos 3 at the different sites, plotted against the TSLM: (a) pH; (b) NH3 (mg kg1 TS); (c) TS (%) and (d) VS (%); p and 95% confidence interval levels displayed in graphs.

C.H. Lalander et al. / Waste Management 33 (2013) 2204–2210

10

8

6

4

2 R2 = 0.31 p = 0.016

0 6.6

6.8

7.0

7.2

7.4

pH Fig. 6. SolvitaÒ maturity index plotted against the pH; R2, p and 95% confidence interval levels displayed in graph.

appear that vermicomposting can accelerate the reduction of coliphages; rather, the good correlation between coliphage concentration with TSLM and the poor correlation with pH indicates that the reduction of coliphages is natural and time dependent. However, more research is required for a better understanding of the fate of viruses in the vermicomposting process.

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fertiliser (e.g. cucumber that is very close to the ground compared to corn that grows above ground). A 1 log10 reduction is assumed when incorporating the fertiliser into the soil, a 1 log10 reduction for a crop growing above ground and a 2 log10 reduction for peeling fruits and vegetables. In these UDVTs, the averaged reduction from pos 1 to pos 3 was 1.5  2 log10 for TTC, Ent. spp. and coliphages based on information from all sites visited (Table 1), keeping in mind the great variation within each position between the different sites. As discussed above, additional reductions can be expected at pos 3. For instance, the concentration of Ent. spp. varied up to 3 log10, based on the pH and hence maturity of the material. The concentration of TTC varied up to 1 log10, while the concentration of coliphages varied 4 log10. The hygienic quality of the vermicomposted material could be improved by introducing a fourth, maturation point, onto which the material at pos 3 could be placed prior to relocating the material at pos 1 to pos 3. At the maturation point the material would be allowed to mature without the risk of recontamination and with minimised risk for regrowth, as regrowth is less likely in matured material (Elving et al., 2009). With a fourth, maturation point, a potential total reduction of 5 log10 could be achievable for Ent. spp., a 3 log10 reduction for TTC and a 6 log10 reduction for coliphages, in these systems. As the reduction of TTC was the smallest it is the limiting factor, restricting possible reuse opportunities. For reuse of crops consumed raw an additional sanitisation step would be required. Ammonia sanitisation is a potential treatment option that ensures hygienically safe material with increased fertiliser value (Winker et al., 2009).

3.4. Factors affecting compost maturity at pos 3 The current practise of piling fresh material onto the already vermicomposted material (shifting material in pos 2 to pos 3) poses a serious risk not only for recontamination of stabilised material, but also for regrowth of pathogenic bacteria. It has been demonstrated that the regrowth of bacteria is considerably higher in active compost compared to regrowth in inactive compost (Elving et al., 2009). The authors used the SolvitaÒ index for compost maturity to define active and inactive compost. Additional factors, not taken into account in this study, affects the maturity of the vermicompost (pos 3) in this system, e.g. the average ambient temperature and the yearly number of users. Site 6 was the toilet located at the highest elevation (2160 m AMSL). Great part of the year no degradation take place as the material is mostly frozen, which will affect the time it takes to reach maturity and thus the reduction of bacteria. At this site the concentration of coliphages was very low, although the concentration of TTC and Ent. spp. was high and the material had not been properly degraded, demonstrating again that the reduction of virus particles most likely does not correlation with material maturity. The yearly number of users and thus the amount of material generated at each site will also have a great effect. In conjunction to this, the way by which maintenance is conducted – the amount relocated and the frequency of relocation from pos 1 to pos 3 – could impact. No standardised maintenance manual exist about when the material in pos 1 should be relocated, but rather depend on the judgement of the operator. 3.5. Reuse potential of vermicomposted toilet material According to the WHO guidelines on reuse of excreta in agriculture (WHO, 2006), a 6 log10 total reduction of bacteria (correlated to E. coli concentrations) is required. The sum of all reductions in risks are taken into account, such as: the treatment, the way by which the fertiliser is distributed (mixed into the soil or placement onto the soil without incorporation), the type of crop fertilised (crops consumed raw or cooked) and the crops distance from the

4. Conclusion This study demonstrate that UDVTs systems are a viable option for on-site management of human waste. In the studied toilets it was found that the vermicomposted material was odour free, homogenised and possible to reuse for crop production. The accumulation of material in the toilets was kept down to a minimum, as the earthworms effectively reduced the material mass. As UDVTs do not require much maintenance, they are ideal for installation in remote locations. The factor found to correlate to the concentration of bacteria was the pH, indicative of the material maturity. The factor found to correlate to the concentration of coliphages was the TSLM, as the reduction of these are believed to be natural and time dependent. An improved set-up of the current system, in which a maturation point is introduced, could improve the hygienic quality of the vermicomposted material. However, as the reduction of TTC was not sufficiently high, fertilisation of crops consumed raw would, if following WHO guidelines, only be possible if introducing an additional sanitisation step.

Acknowledgement The study was supported by the Swedish Ministry of Foreign Affairs as part of its special allocation on global food security and by the National Science and Engineering Research Council of Canada. The authors would like to thank Ecosphere Technologies for all the help and support during sampling.

Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.wasman.2013.07. 007.

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