Application of solarization for sanitization of sewage sludge compost

2.1 Collection and preparation of sewage sludge

The sewage sludge used in the experimental study was collected from a Wastewater Treatment Plant (average wastewater flow rate = 80,000 m³ day⁻¹) of the city of Sakarya, located in the northwest region of Turkey (latitude 40° 50′ N, longitude 30° 19′ E, and 31 m above the sea level). The treatment plant is operating with extended aeration. After thickening process, sludge is mechanically dewatered by decanter, allowing about 20% dry matter content. The dewatered sludge obtained from this facility was first composted in a 60 L-capacity laboratory-scale composter by mixing with 1:1 (v/v) grounded hazelnut husk (particle size of 0–4 mm) bulking agent. The composting experiment was carried out for a period of 28 days, representing the active composting phase. No specific aeration system was installed, but pile was aerated by mixing the content manually every day. Temperatures of the compost pile were above the 52 °C threshold during 3 days of the first 15 days of the composting experiment. The initial concentrations of selected indicators in compost mixture were 4.0 log CFU g⁻¹ for E. coli, 5.1 log CFU g⁻¹ for thermotolerant coliform, 2.31 log CFU g⁻¹ for Enterococci, and 4.0 log CFU g⁻¹ for Clostridium.

Following the active phase of composting, compost samples were homogeneously separated into parts. One part of compost sample was loaded into the PVC solarization container up to a height of 40 cm. Solarization treatment was directly exposed to ultraviolet radiation provided by sun at local environmental conditions, while unsolarized (control) treatment, which was conducted with the same amount of compost, was kept at room temperature (25 ± 2 °C) in the laboratory during the experimental study (Fig. 1).

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Fig. 1

Schematic representation of the solar application to sludge compost for microbial disinfection.

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2.2 Sampling period and procedure

The experiment was carried out from August 1 to 15, 2015. Meteorological data of the experimental period were obtained from Adapazari meteorological station, Sakarya, Turkey (Fig. 2). Compost temperatures at two different depths (between 0–10 cm and 10–30 cm) were measured on a daily-basis (every day 14:00p.m.) by using a soil thermometer (TF002, Agromak, Turkey) within two-week sampling period. Compost samples were taken from 5 and 30 cm depths in each sampling day and homogenously mixed sub samples obtain from mixture were used for microbial analysis. The effects of solarization on microbial reduction were evaluated by obtaining samples (1 g for each treatment) at every 48 h within 15 days of the entire experimental period.

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Fig. 2

Ambient solar radiation, the maximum and the minimum daily temperatures during the solarization period.

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2.3 Indicator microorganisms and microbial procedure

For quantitative evaluation of the microbiological quality of sludge compost and the sanitation efficiency of the present solar application, Escherichia coli, thermotolerant coliforms, Clostridium, and Enterococci were chosen as the indicator microorganisms. In this study, Escherichia coli and thermotolerant coliforms were identified on m-FC medium following to the membrane filtration based on the procedure specified in ISO 9308-1 (ISO, 2014). Enterococci was enumerated by membrane filtration in accordance with the ISO standard 7899-2 (ISO, 2000). Moreover, Clostridium was counted based on ISO 14189 standard (ISO, 2013).

Serial dilutions of the sample were performed in the isotonic solution, and 1 g of each sample was consecutively diluted tenfold in 9 mL of this solution for the microbial analysis. Dilutions from 10⁻¹ to 10⁻⁵ of 100 μL of 1:10 dilution were conducted in triplicates on different microbiological media. The inoculated plates were incubated at 37 °C for 24 h, after incubation, the emergent microbial colonies on each plate was quantified and each value was recorded (Ogleni and Ozdemir, 2010).

2.4 Microbial inactivation modeling

For the quantification of decline in survival curves, the following shoulder/tail inactivation models (i.e., linear approach, logistic (or Fermi) function, and residual population density-based inactivation model, respectively) expressed in Eqs. (1)–(3) are used (Geeraerd et al., 2000; McKellar and Lu, 2003; Sant’Ana, 2016):

In this study, GInaFiT inactivation model fitting tool was implemented to derive the best-fit microbial inactivation models for the selected indicator microorganisms (Geeraerd et al., 2005). The analyses were implemented within the framework of GInaFiT version 1.6 a freeware Add-in for Microsoft® Excel® 2016 (Microsoft Inc., Redmond, WA) package operating on a Casper Excalibur (Intel® Core™ i7-7700HQ CPU, 2.81 GHz, 16 GB of RAM, 64-bit) Windows 10 PC platform. In all calculations, spreadsheets of Microsoft® Excel® running under the same operating system was used as an open database connectivity data source. According to the preliminary computational analysis, the best-fit models were log-linear regression, log-linear regression plus tail, and log-linear regression plus shoulder plus tail, respectively, for E. coli, thermotolerant coliforms, and Enterococci and Clostridium.

2.5 Statistical procedure

In this study, the root mean sum of square error (RMSE) was used as the primary statistical performance indicator for judging the quality of the best-fit inactivation curves. The inactivation rate k_max (slope of the exponential portion of the survival curve) and T₉₀ values (time to inactivate 90% of the population) were computed using the best-fit models obtained with the help of GInaFiT. Log₁₀ transformed bacterial quantifications were subjected to two-way analysis of variance (ANOVA) analysis to interpret the influence of time and sludge depth on the pathogen inactivation. In the computational analysis, an alpha (α) level of 0.05 (or 95% confidence) was considered to appraise the statistical significance of the shoulder/tail-based models.

The data sets of solarized and unsolarized (control) treatments obtained for indicator microorganisms were statistically evaluated via proper parametric (unpaired (or two-sample) t test and F (variance ratio) test) or non-parametric tests (the Mann–Whitney (MW) U (or the Wilcoxon rank-sum) test or the Kruskal–Wallis (KW) test with the Dwass-Steel-Chritchlow-Fligner method). Prior to applying these tests, the Shapiro–Wilk W and the Levene’s tests were respectively implemented as preconditions to ensure whether the subsets (herein solarized and unsolarized treatments for indicator microorganisms) had a normal or non-normal distribution, and variances (or standard deviations) of the paired groups were homogeneous or unequal. In case of the data sets were not normally distributed, a non-parametric test (MW or KW) was conducted instead of a parametric test. Test results were appraised with two-tailed p values to indicate the statistical significance between the experimental groups (Ozdemir et al., 2020).

3.1 Temperature increase by solarization process

The variation of temperatures recorded at the depths of 5 and 15 cm in the solarized compost during the experimental period is depicted in Fig. 3. As seen from the respective profiles, at the beginning of the solarization process, the temperature quickly rose above 50 °C on day 3 for both monitored compost depths. During the days with higher solar radiation, compost temperatures were recorded above the thermophilic temperature of 60 °C at 30 cm depth and even reached 65 °C at 5 cm of compost depth. As expected, those compost temperatures were significantly higher (p < 0.01) than the compost kept at laboratory conditions. Compost temperatures in unsolarized experiment were close to ambient temperature fluctuated around 20–25 °C at each sampling day. For 2-week summer term, solarization of compost in the PVC container was very effective for increasing the compost temperature (Fig. 3) and showed a lethal effect for E. coli, thermotolerant coliforms, Enterococci, and Clostridium species (Romdhana et al., 2009; Sossou et al., 2016).

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Fig. 3

Recorded compost temperatures at 5 and 30 cm depths of solarized treatment during experimental period.

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3.2 E. coli inactivation

The driving force of time-temperature kinetics has been known as the main process for bacterial inactivation in heat applications for sanitization experiments (Singh et al., 2011; Sossou et al., 2016). In a laboratory-scale time–temperature experiments, Lang and Smith (2008) examined the bacterial decay of E. coli strains at 70 and 55 °C and found the complete inactivation after 10 s and 20–60 min respectively. However, in a full-scale processing conditions, complete inactivation time was reported to be extended beyond the hours to day in thermophilic temperature ranges (Singh et al., 2011). In the present study, E. coli population decreased rapidly under the solarization treatment, and the reduction rate showed a first-order (linear) removal kinetic with substantially higher reduction effectiveness at solarized compost samples compared to the unsolarized treatments (Fig. 4a). E. coli population was reduced from 4 log CFU g⁻¹ to below the detection limit values of 2 × 10¹ cells (as CFU) after 6 days of solarization. The number of E. coli of compost samples that did not exposed to solarization reduced, but the reduction rate was determined to be less than the 1-log. The results indicated that the temperature increase in solarized compost samples was caused a lethal temperature range for E. coli. Consistent with previous researches, E. coli was more susceptible to heat inactivation (Watcharasukarn et al., 2009) assured by the solarization. For the increasing temperatures, the inactivation kinetics (k_max = 1.04 day⁻¹ and T₉₀ = 2.91 days) obtained in the present study were agreed with those observed for the E. coli in the similar solarization conditions applied for the municipal sewage sludge (k_max = 0.65–0.85 day⁻¹ and T₉₀ = 2.47–4.60 days) depending on sludge depth (Ozdemir et al., 2013). The reductions in the number of microorganism showed a positive correlation with time. On the other hand, compost temperatures were induced by higher ambient temperature and daily solar radiation level. Therefore, inactivation rates (k_max) increased with compost temperature increase, and T₉₀ values reduced (Table 1). The numerical results corroborated the positive impact of the solarization on inactivation rate of E. coli.

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Fig. 4

Inactivation of indicator microorganisms in the sludge compost under solarized and unsolarized treatments: (a) E. coli; (b) Thermotolerant coliforms; (c) Enterococci; and (d) Clostridium.

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3.3 Thermotolerant coliform inactivation

As seen from Fig. 4b, the number of thermotolerant coliform decreased rapidly and was quantified below 1-log after 6 days of solar application, while the population in unsolarized (control) treatment remained almost stable during the experimental period (Fig. 4b). The average number of thermotolerant coliforms was quantified as 5.10 log CFU g⁻¹ at the beginning of the solar application and reduced substantially to 1.01 log CFU g⁻¹ within the first week of the process. After the bacterial concentration decreased to 1.01 log CFU g⁻¹, the rate of destruction within the further stage was recorded to be slower. This can be ascribed to the fact that heat resistant fraction of the bacteria need be exposed to higher dose of inactivation factor with longer exposure time. This is compatible with the findings of Lang and Smith (2006) who reported the complete inactivation of thermotolerant strains within 40 s and 60 min at 70 and 55 °C, respectively. Representing the real-world applications, the complete inactivation was achieved on day 15 at the end of the experimental period of present study, which is in line with the Singh et al. (2011) who reported more than 5 days for complete removal from compost mixture at 55 and 60 °C. For the thermotolerant coliforms considered in this study, a positive correlation (p ≤ 0.01) between bacterial reduction kinetics and temperature rise achieved by the solarization confirmed the desired sanitizing condition for the sludge compost (Ogleni and Ozdemir, 2010).

3.4 Enterococci inactivation

Unlike E. coli and thermotolerant coliform, the number of Enterococci bacteria in the sludge compost remained almost stable (except with a very small fluctuation from 2.31 log CFU g⁻¹ to 2.30 log CFU g⁻¹ for solarized treatment) within 3 days of the entire experimental period (Fig. 4c). The initial mild temperatures and appropriate compost substrates were considered suitable conditions for the viable cell count for those bacteria species. The viable cell counts of Enterococci revealed that the viability of these bacteria with time ranged from 2.31 log CFU g⁻¹ to 1.80 log CFU g⁻¹ for solarized compost (within 6 days) and decreased to concentrations below the detection limit of 2 × 10¹ cells (as CFU) after 12 days of solar application. The destruction of the indicator organisms could be explained by the increase in temperature and other possible environmental conditions (Ozdemir et al., 2013). The reduction of the Enterococci count below the detectable number was noted after 12 days of solar application. Supporting results were also observed by Klein et al. (2010) who reported rapid inactivation of Enterococci at 60 °C (k_max = 1.2 day⁻¹ and T₉₀ = 2.1 days) compared to the incubation at 37 °C (k_max = 0.05 day⁻¹ and T₉₀ = 46 days).

3.5 Clostridium inactivation

Clostridium was selected as another indicator microorganism to determine the effect of the implemented solarization process to removal kinetics of resistant bacterial species. The removal rate during the solarization is shown in Fig. 4d. The decrease in viable cell under the solar application was found positively correlated with the temperature rise (p ≤ 0.01). While the solarization treatment provided 3-log reduction, the Clostridium reduction in unsolarized treatment was determined as 0.7-log. However, according to the inactivation curves, T₉₀, and k_max values (Table 1), the Clostridium was found to be more resistant to heat inactivation provided by solarization. It is noted that the sigmoidal inactivation curve, which indicates the resistance of this microorganism to negative environmental conditions, has also been reported by others (Viau and Peccia, 2009; Fisher and Phillips, 2009). Moreover, Usui et al. (2017) reported that temperature rise beyond 55, 60, and 70 °C and exposure times of 5, 10, and 30 days had a positive correlation with the complete elimination of Clostridium bacteria in the sludge.

Although the significant reductions were achieved in viable cell counts, solar application was not able to lower the Clostridium population below undetectable levels of 2 × 10¹ cells (as CFU) (Table 1, Fig. 4d). The possible reason can be ascribed to the adaptive characteristics of the remained fraction of these species to thermophilic conditions, where temperature rises were not faster. Miller et al. (2009) reported that gradual temperature increases stimulate the adaptive mutation, as indicated by the existence of tailing in the inactivation curve. Similarly, presence of heat-adapted strains of Salmonella spp. in a manure compost maintained at 55 °C were observed during the 30 days of experimental period (Shepherd et al., 2010). In the present study, the positive correlation between the temperature rise and 3-log reduction in the number of Clostridium indicated that the solarization process could be applied as a suitable sanitization alternative for the sludge compost.

3.6 Sustainable advantages of solarization for disinfection of organic waste

The municipal wastewater treatment operations generate substantial amount of sludge that should be properly disposed (Alvarenga et al., 2016; Davis et al., 2016). This nutrient-rich sludge could be beneficially recycled for agricultural purposes after composting to meet nutrient demand and enrich the soil organic matter (Boudjabi et al., 2019). Adapting more sanitized sludge compost to crop cultivation is believed to promote recycling facilities, encourage waste management, and land application (Ozdemir et al., 2013; Belloulid et al., 2017). In this regard, considering the combined advantages of waste disposal and the extended beneficial recycling alternatives, integration of composting with environmentally friendly solar disinfection practices might be very feasible for the closed waste management strategies (Davis et al., 2016).

Solarization is an efficient sanitization option to produce microbiologically safe compost, however, the method needs to be further tested for different pathogenic microorganisms and their resistant species such as spore-forming bacteria. Moreover, regardless of the efficacy of the sanitization process, it is also considerable to be aware of the fundamental microbial principles when studying on waste products, such as sewage sludge, to minimize the recontamination that is caused by pathogenic microorganisms.

In this study, a new disinfection alternative for sewage sludge compost using solar energy was introduced, and its performance was analyzed by focusing on different indicator microorganisms in the summer period of temperate region. In the future studies, system performance could be analyzed in terms of different environmental conditions such as compost humidity, CO₂ concentration, or solar radiation rate. More detailed configuration could be developed by the designer for the aim of increasing the temperature rise and accumulation of heat in the solarization system to define technical options that enable to achieve higher performance.