Application of the Sewage Sludge in Agriculture: Soil Fertility, Technoeconomic, and Life-Cycle Assessment

Abstract

Disposal of sewage sludge, which is a by-product of wastewater treatment, has become one of the greatest challenges of the twenty-first century. Conversion of sewage sludge to a soil amendment can be performed by a broad spectrum of methods, which greatly differ by substrate/amendment composition, treatment time, and physicochemical conditions. The book chapter is focused on (i) environmental and legislative aspects of sewage sludge application in agriculture; (ii) risk factors related to the abundance of pathogens in sewage sludge and methods of SS hygienization; (iii) optimization of the use of SS-derived fertilizers. Application of sewage sludge in combination with mineral fertilizers positively influenced crop growth and soil microbiological activity. An environmental impact of sewage sludge related to its disposal to agricultural areas has been analyzed in terms of global warming, ecotoxicity, and other internationally recognized issues. Narrowly targeted measures may aggravate the situation. Some site-specific factors make sewage sludge unique, hence this specificity must be considered to predict the outcome of its treatment. Determination of these factors remains challenging. Therefore, the complexity of sewage sludge can be reduced by employing integrated biorefinery approaches that will result in circular bioeconomy and industrial ecology solutions.

1. Introduction

Sewage sludge (SS) is formed as a by-product at a wastewater treatment plant (WWTP) and represents a heterogeneous mixture. This complex suspension consists of solid organic and inorganic substances and colloids, which have been separated from the wastewater during the treatment process [1]. The global production of SS is estimated at 45 million t of dry matter per year [2, 3]. During the last decade the SS production in EU countries increased by 1.5 million t of dry matter (DM), that is, from 11.5 million t in 2010 to 13 million t in 2020 [3], therefore, its management is a problem of great concern. The SS disposal reaches up to 60% of the total operating costs of WWTP, and, hence, makes this process problematic and expensive [4].

Sludge from WWTP is recovered by compost production, the application directly to agricultural and forest land, production of growing substrates, and energy recovery [5]. For practical and legal reasons, SS is increasingly reused rather than landfilled. This approach aims to minimize generated waste and promote the development of the bioeconomy that provides intelligent waste management, and, hence, is consistent with zero-waste strategy [3, 6]. Different countries have chosen different strategies for the use of urban SS. Analysis of the Eurostat data in the period from 2014 to 2018 showed that the use of SS in agriculture, in combination with compost, had been the main route for sludge disposal in the EU with 44.58%, followed by incineration (32.70%) and other methods of disposal (9.16%). Landfill disposal was at the level of 7.81%. Comparing the costs of different sludge disposal methods, the application on land and agriculture involves the lowest cost compared to composting, drying, incineration, and landfill.

At WWTPs, with more than 10,000 inhabitants, the sludge is divided into primary and secondary sludge. The primary sludge contains settling substances (from primary settling tanks), usually, it has a granular structure. Secondary sludge, also called excess sludge, consists of a mixture of microorganisms and settable substances from the biological stage of the WWTP. Primary sludge and secondary sludge are referred to as so-called raw sludge. The raw sludge is still microbially active, it can contain pathogenic microorganisms, with the total content of organic substances in the dry matter at about 70%. However, dewatered sludge (20–45% DM) is considered harmless and suitable for agriculture, because of high content of organic matter and biogenic elements (C, N, P), which increases soil fertility and is essential for plant growth and development as well as for soil microbiota [1]. Therefore, the use of SS on agricultural land is the best way to recycle the nutrients it contains, thus making the SS an important biological resource for sustainable agriculture [7, 8, 9]. On the other hand, the application rate is of great importance. Excessive concentrations of plant nutrients, mainly nitrogen and phosphorus, can also harm the environment, especially inland waters.

Another important issue is related to the abundance of hazardous and very persistent substances, such as heavy metals, polycyclic aromatic hydrocarbons, polychlorinated biphenyls, halogenated hydrocarbons, polychlorinated dibenzo-p-dioxins and dibenzofurans, pesticides, personal care products, hormonal substances, drugs and their metabolites, microplastics, and nanoparticles [8].

Therefore, the incorporation of sludge and its compost in the soil is regulated by various legislative acts [9]. The annual emission limit values for dry matter, heavy metals, total nitrogen, and total phosphorus are the maximum mass of these substances that can be applied per hectare of sludge or compost on average per year. Emission limit values for sludge dry matter vary considerably between the EU Member States, ranging from 1 to 10 t ha⁻¹ per year. According to Mercl et al. [10], a high rate of SS composts applied once (60 t ha⁻¹ compost in seedbed) is not recommendable since high nitrate concentration is not taken up by maize and increases the leaching risk. Furthermore, SS commonly contains high amounts of human pathogenic bacteria excreted in feces and urine, so the SS should be appropriately hygienized before application in agriculture.

The aim of this chapter was to summarize the main aspects of SS treatment for its application in agriculture, with emphasis on process efficiency, safety, and feasibility. The dual role of SS as a fertilizer and amendment in the soil is widely described in the literature, referring to the supply of nutrients to plants and improving the soil’s physical conditions, respectively. Our own results on SS treatment have been incorporated into the review of recent scientific literature and legislative documents.

2. Characteristics of sewage sludge as a potential soil amendment/fertilizer

Sludge is rich in organic matter, nitrogen, phosphorus, and other macro and microelements, which makes it a useful raw material to be used in agriculture. Dry SS contains on average 50–70% organic matter and 30–50% mineral components [8]. Physicochemical and biological characteristics of agricultural soils, which are amended with the organics-rich SS, can be considerably improved. Particularly, a reduced bulk density leads to an increased soil porosity and soil-air recirculation, as well as improved soil structure and water holding capacity. Besides, the concentration of soil humus is increased. Organic matter of SS enhances soil nutrient storage, soil biota, and diversity, as well as reduces exposure to erosion. High organic matter content facilitates the formation of stable organic complexes with humic acids, thus reducing metal availability [11]. A slow release of mineral elements from SS to soil also changes the physical, chemical, and biological parameters of soil and benefits from increased gas exchange, better water infiltration, and its retention. The compounds of SS are available for a longer period [12].

Mbagwu and Piccolo [13] found that the decomposition of organic materials in sludge enhances the availability of nutrients such as nitrogen and phosphorus substantially. Application of SS at a rate of 200 t ha⁻¹ increased the total nitrogen of soil aggregates by 57% and available phosphorus by 64.2%.

The formation of organic and inorganic acids throughout the decomposition process of SS components under aerobic conditions increases soil acidity. Soil salinity positively correlates with the increased application rate of SS. Amendment of loamy-clay soil with SS at dose 60 t ha⁻¹ increased soil carbon content from 0.16% to 1.45% [14].

Comparison of physicochemical characteristics of SS of different origins showed that average concentrations of nitrogen, phosphorus, and potassium are similar and reach up to 3.20%, 1.75%, and 0.5% per kg of treated dry SS, respectively [15, 16, 17]. Often the potassium content in SS is considered insufficient for plant nutrition [8]. Some studies indicate that SS is an efficient replacement for chemical fertilizers, especially phosphorus. Indeed, Switzerland, Germany, and Austria are developing legislation to make P recovery mandatory from municipal SS [18, 19].

Nevertheless, there are some site-specific factors (e.g., applied technology, quantity, and the origin of raw wastewaters, which differ by the composition of macro- and microelements and risk compounds), that make each SS unique, hence this specificity must be considered to predict the outcome of SS treatment. Determination of these factors remains challenging [20].

3. Legislative aspects in the use of sewage sludge in agriculture

The management of SS in the EU is regulated by various legislative acts. The Directive 2008/98/EC establishes the fundamental ideas and terminologies, such as waste, recycling, and recovery [21]. It explains the basic concepts of waste management, the distinction between waste and secondary raw material (“end-of-waste criteria”), waste, and by-products. The directive lays down basic principles of waste management without adversely affecting human life, health, nature, and the environment. Waste legislation and policy of the EU Member States shall apply as a priority order with the waste management hierarchy (Figure 1).

Figure 1.

The Waste Framework Directive 2008/98/EC priority order with the waste management hierarchy [21].

SS dose/soil	Plant species and effect	Reference
Field experiments
8.3% w/w/clayey–silty	Yield increase by mulching 65.7%, by mixing 91.5%: wheat (Triticum durum)	[78]
15, 30 and 60 t ha^−1/Entisols	Grain yields at the 1st year less than mineral fertilizers by 3–5%, 2nd year increase in average by 13.8%: corn (Zea mays)	[12]
20 t ha^−1/clayed soils	Grain yield increase by 71–171%: wheat (Triticum sp.)	[79]
25 t ha^−1/n.d.	Yield increase by 43.5%: radish (Raphanus sativus)	[80]
30 t ha^−1/n.d.	Yield increase by 26%: sunflower (Helianthus annuus)	[81]
40 t ha^−1/sandy clay loam	Grain yield increase by 91.6%; 1000-grain weight increase by 26.9%; number of productive tillers by 51.4%: wheat (Triticum sp.)	[82]
80 t ha^−1/calcareous soils	Head yield increase by 186%: lettuce (Lactuca sativa)	[83]
150 t ha^−1/n.d.	Increase by 42.3% in comparison with control, decrease by 31.8% in comparison with RDMF, that is, 45.5% and 22.1%; 46.3% and 18.9%; 51.6% and 27.8%; 52.1% and 8.5%; 35.5% and 16.2%: carrots (Daucus sativus); turnips (Brassica rapa); radish (R. sativus); tomatoes (Solanum lycopersicum); onion (Allium cepa); summer squash (Cucurbita pepo), respectively	[84]
250 t ha^−1/mudflat saline-alkaline soil	Biomass increase by 399.7% (control 1.3 t ha^−1): sweet sorghum (Sorghum bicolor)	[85]
Vegetation pot experiments
40 t ha^−1/loamy clay (calcareous)	Increase of DM up to 5%: barley (Hordeum vulgare)	[86]
30 t ha^−1/alluvial soils	Seed cotton yield (71.4%), lint yield (67.7%), and cottonseed yield (74.1%) were increased: cotton (Gossypium hirsutum)	[87]
300 t ha^−1/mudflat soil	Fresh weight of aboveground parts and roots increased by 555 and 128%, respectively: ryegrass (Lolium perenne)	[88]
15 and 30%, v/v/peat-based medium	Pepper yield and the number of fruits per plant increased by 28–43 and 30–98%, respectively: pepper (Capsicum annuum)	[89]
50%, 100%, and 150% of RDMF	Total sugar and sugarcane increased by 4.68 and 4.19%: sugarcane (Saccharum officinarum)	[90]
50 and 100%/soil loamy chernozem	Chlorophyll b (15–38%), carotenoids (5–50%) increased, while plant fresh weight (100%) SS was decreased by 8%: Sweet basil (Ocimum basilicum)	[91]
8.7 g L^−1 + MF/loamy sand	Yield increase by 15%: corn (Zea mays)	[73]
10, 20, 30, and 40 g kg^−1/n.d.	Seed germination rate increased by 9.6, 19.0, 28.6, and 28.6%, respectively, total biomass increased by 146, 236, 278, and 400%: broad bean (Faba sativa)	[14]

Table 1.

Plant growth in response to the presence of SS in soil.

RDMF: recommended dose of mineral fertilizers; MF: mineral fertilizers.

An ex-post evaluation of the SS Directive 86/278/EEC in 2014 showed that its initial objectives were achieved, in spite of large variations in the amount of SS used in agriculture in the Member States (from none to well over 50%) [21, 22]. Currently (2020–2021), the EU initiated an evaluation of legislation efficiency, as well as the risks and opportunities of SS used in farming [23, 24].

Furthermore, two EU working documents on sludge have been produced: the EU Working Document on sludge (2000) and the EU Working Document on sludge and biowaste (2010). The EU Working Document on sludge (2000) indicates that to be used without restrictions, sludge should undergo an hygienization process by an “advanced treatment,” which should result in at least a 6-log-unit reduction in Escherichia coli, as well as create a sludge that meets the following criteria: In 50 g, there is no Salmonella (wet weight, WW) and E. coli <500 colony-forming unit CFU g⁻¹. It was also proposed that sludge produced by “conventional treatments” should show a 2-log-unit reduction of E. coli, and its use is allowed with restrictions on its application time, site, and modality. Mesophilic anaerobic digestions at a temperature of 35°C with a mean retention time of 15 days and thermophilic anaerobic digestions at a temperature of at least 53°C for 20 h as a batch, without admixture or withdrawal during the treatment, are indicated, among others, as conventional and advanced treatment processes, respectively. The more recent EU document only suggests the limited absence of Salmonella in 25–50 g and E. coli <5 × 10⁵ g⁻¹ WW as possible criteria for the use of sludge in agriculture [25].

According to the EPA Environmental guidelines published in 2000 on stabilization of biosolids products [26], a biosolids product must meet at least one pathogen reduction requirement and at least one vector attraction reduction requirement [27]. Stabilization Grade A includes thermally treated biosolids (at least 50°C), high pH-high temperature process and biosolids from unknown processes, while stabilization Grade B—anaerobic digestion, aerobic digestion, air drying, composting, lime stabilization, extended aeration, and other processes accepted by the EPA products [26].

4. Economical aspects: technological efficiency and circular economy

In the context of sustainable development principles some main components, which determine the rational solution of the multi-faceted problem of municipal SS, must be considered. Poor farming practices combined with the overuse of chemical fertilizers on poor soils have caused a negative environmental impact, which leads to the degradation of arable land. The effort to increase productivity by increasing the use of various chemicals in fertilizers further diminishes soil fertility. With each harvest, the soil loses organic compounds, and permanent aggravation of improper agricultural practices often prevents the land from recovering. World chemical fertilizer consumption increased from 70.95 kg/ha in 1976 to 138.16 kg/ha in 2016. And in some regions, the fertilization dose increased up to hundreds and even thousands of kilograms per hectare (Figure 2) [28].

Figure 2.

Fertilizer consumption by different countries and regions. (a) Data on some countries and regions with fertilizer consumption below 500 kg/ha; (b) data on countries with rapid growth of fertilizer consumption, which exceeded 500 kg/ha [28].

The quantity of organic elements in the soil constantly decreases. A significant part of the SS does not return to the soil, but is disposed into the sea, is incinerated, or is subject to other different kinds of destructive effects, leading to drastic decreases in soil fertility and continuous soil degradation.

The quantity of the SS constantly increases. The peculiarity of SS lies in its multi-mineral compound and a huge range of organic matter; in fact, the SS is a nitrogen-phosphorus-potassium organic fertilizer, containing a full set of microelements necessary for the growth of crops. However, due to the high risk of pathogenic impact, a huge part of human and material resources is directed to the destruction of this important resource.

The overwhelming majority of the SS disposal methods are expensive, harmful, or contain both factors. Most municipalities face the growing problem of wastewater treatment. In many cases, waste is dumped into landfills, oceans, or incinerated. The rational solution to the problem of municipal SS disposal lies in an integrated approach to returning the sludge into the agricultural cycle [29].

The directive introduces the “polluter pays” principle and the extended producer responsibility. Some existing projects of producing energy, for example, biogas, minerals, and chemicals out of the sludge, do not prove to be sustainable and viable financially. Furthermore, in most cases, most of the sludge is eventually dumped at the end of the process. Incineration represents the total elimination of the sludge but is extremely expensive. It seems to be the most rational to consider SS not as a problem, but as a valuable resource.

In recent years, out of concern for the profound soil degradation, a growing trend of shifting to organic fertilizers is taking over within the agricultural industry.

The global fertilizer market was valued at around $360 billion before the COVID-19 pandemic with organic fertilizer making up just $6.8 billion. The organic fertilizer market is described as steadily increasing and expected to post a CAGR (Compound Annual Growth Rate) of 14% during the period 2019–2023, with the key factor being increased food demands and agricultural shortages due to population growth and climate change [30].

In case of the continuing negative influence of the high transport, logistics, and energy costs, the SS processing can offset the lack of fertilizers through a domestic product that costs only a fraction of the price to make, creating a local commodity with a considerable economic edge.

Sewage sludge is a natural epidemic focus, and the detection of SARS-CoV-2 in fecal masses led to the long-overdue conclusion to strengthen human health protective measures and counteract the emergence of epidemics [31]. The necessity of the implementation of new biological safety criteria can have a significant economical and long-term structural influence on the development of the entire sphere of processing and use of SS. For instance, regarding the sediment formed during the epidemic, it is recommended to avoid its traditional aerobic composting. At once, in the sludge undergoing thermal disinfection treatment, the risk of infection with SARS-CoV-2 is considered in the range from low to negligible [32]. Intensive decontamination measures will make the product more expensive, but more in line with the requirements of sustainable development.

To prevent potential biological threats toward the environment and human health, it becomes increasingly important to develop the most isolated from the environment hermetic methods for the SS disposal, without destroying the organic component, valuable for agriculture.

Economic aspects of SS hygienization have been analyzed [33]. The energy requirement per 100 tons of sludge was estimated depending on different disinfection conceptions. Thus, solar dehydration and chemical treatment with alkali consume 11.7 and 148.3 kW h with the production of 80 tons and 99.6 tons, respectively. In turn, the most expensive technology is gamma irradiation, which consumes 64,800 kW h for obtaining 97.6 tons of the product. The thermal drying also requires quite a high energy consumption, that is, 21,000 kW h for 20 tons of product. The composting does not consume electricity [33]. The high costs of thermal hydrolysis and ultrasonic methods and the need for a neutralizing agent in acid solubilization limit the rapid implementation of these processes in industrial practice [34].

Our testing of the infrared heating method for SS disinfection demonstrated successful results. It took 15 min for the material with an 80% humidity, including the time it required to heat the layer to 95°C, which is below the temperature at which the organic matter decomposes [35].

The widespread usage of SS biomethanation has resulted in the building of a number of complex installations that combine biological wastewater treatment facilities with anaerobic digesters. The development of digestate-derived granulated soil fertilizers is based on physicochemical processing of biostabilized sludges, in keeping with the circular economy concept and the concept of “waste-to-product” [36].

In this respect, the costs of pretreatment technologies for SS biomethanation with further conversion of digestate to fertilizers should be taken into consideration. The estimated energy utilized for the mechanical operations during SS disintegration and anaerobic digestion (stirring and pumping) was calculated to be 1253.6 kW h per ton [37]. The energy spent for SS pretreatment may vary depending on the solubilization [38], used consumables [39], and methods [40]—thermochemical (TC), sonic, thermo-chemo-sonic, etc. It is experimentally proven that combined disintegration pretreatment should be more efficient. The energy consumption for TC sludge pretreatment (30% solubilization) for biogas production was calculated to be 1588.552 kW h per ton of sludge. The thermos-chemo-ozone (TCO3) pretreatment can optimize the total energy input up to ~721.766 kW h per ton [41].

The evaporation of water should be weighed out between the energy costs in the process and the SS management costs without drying [42].

According to the economic feasibility review of our project for fast SS recycling into biological fertilizers, the energy cost will be nearly $30 per ton of fertilizers (with its humidity ~50% and energy costs $0.1 per kW h and initial SS humidity ~80%). The tested method allows providing 1 ton of bio-pathogenic-free fertilizers due to utilizing up to 1.5 tons of SS and withal avoid other SS disposal costs (Figure 3) [43].

Figure 3.

Technology of the fast recycling of SS into organic fertilizer. Methods are according to Chukurna et al. [43].

The applied methods and technical decisions have international priority under the Paris Convention for the Protection of Industrial Property, the World Intellectual Property Organization (WIPO) Eurasian Patent Organization (EAPO) and national patent organizations.

5. Sewage sludge treatment technologies

5.1 Stabilization

Stabilization of SS aims at reducing some disadvantages of SS (e.g., odor, leaching of heavy metals, etc.), thus considerably extending the potential of SS application. The extent to which readily biodegradable organic matter has degraded is referred to as the degree of stability [44]. Mixing of SS with fly ash, lime, peat, clay, straw, and other residues considerably improve SS characteristics, reducing leachability for metals and soil loss [45, 46]. The addition of wheat straw to the bioaugmented SS after 16 days incubation demonstrated the highest and most stable respiration intensity, the lowest ammonia emission, and the highest stimulation effect on the cress seedling growth, as compared to other treatment types [47].

Santos et al. [22] compared the performance of six residues serving for (i) sludge drying and (ii) improving agronomic properties of the final product. Weathered coal fly ash, bottom biomass ash, green liquor dregs, lime mud, eggshell, and rice husk were chosen as adjuvants based on circular economy and industrial ecological parameters. (0.15 g adjuvant/g SS wet basis). The addition of bottom biomass ash to SS promoted the highest diffusion coefficient and drying rate. The highest positive effect on agronomic parameters was shown for the SS amended with eggshell. Among evaluation criteria were acid neutralization capacity, oxygen uptake rate, and germination index [22].

5.2 Disinfection

Sludge treatment technologies for preparing a valuable fertilizer must meet legislative criteria on sludge hygienization. Numerous technological approaches on SS treatment, which were conducted at ambient temperature or under mesophilic conditions, had a strong effect on biological liquid sludge stabilization and natural dewatering and drying technologies, although disinfection efficiency was unsatisfactory [48, 49, 50]. In this respect, further comprehensive research on SS treatment should be focused on a combination of different physical (especially, thermal) and chemical processes, which would convert SS into a qualitative fertilizer with safe microbiological characteristics. Figure 4 summarizes a broad spectrum of methods for SS disinfection. Several studies have experimented with hybrid methods where two or more technologies can be integrated to increase treatment efficiency and performance [62].

Figure 4.

Methods of sludge disinfection. Combination of different methods is indicated by asterisks of the same color. By Izydorczyk et al. [34, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61].

The disinfection approaches should be optimized to minimize potential adverse impacts, such as antimicrobial resistance [62]. Another inherent problem with all sludges rich in nutrients is pathogen regrowth. Offensive odors serve as indicators of microbial regrowth because they are produced as bacteria break down proteins and other organic compounds containing nitrogen and sulfur [63].

6. Changes of microbial community composition in the sewage sludge and soil upon sludge treatment and application

The SS is characterized by a great microbial diversity, which may vary depending on the origin of sewage, its treatment, and industrial activity. Microbial activity in SS, transformation by-products, and residues may impact soil quality if SS is used as fertilizer/amendment [64]. The number of different groups of indicator microorganisms in 1 g of raw SS (wet) on average is 10²–10³ for Salmonella (bacteria), Enteroviruses (viruses), Giardia (protozoa), and Ascaris (helminths), while 10⁶ – for bacteria Escherichia coli [56, 65].

6.1 Microbial community structure in the raw and treated sewage sludge

Many factors modulate microbial community structure within SS, which may change from autotrophic to heterotrophic bacteria depending on the effluent source. According to Nascimento et al. and Nielsen et al. [64, 66], Proteobacteria phylum (21–65%) is predominant in municipal SS. This phylum was primarily dominated by Betaproteobacteria that represents bacteria involved in organic matter degradation and nutrient cycling. Bacteroidetes, Acidobacteria, and Chloroflexi were among the less prominent species. Our recent experiments have also revealed Proteobacteria to dominate in the raw SS (60.17% reads), which consisted of 16.40%, 29.18%, and 12.33% of Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria, respectively. At the genus level, the most abundant were Streptomyces (5.68%) and Pseudomonas (3.48%) (Figure 5A) [47].

Figure 5.

Relative abundance of microorganisms in sewage sludge. A—at the genus level with relative abundance ≥1% (29% from the total reads); B—Salmonella enterica and Escherichia coli in the sewage sludge before and after the 16-day incubation with different carbon amendments. Methods are according to Rimkus et al. [47].

Considerable changes in the microbial community structure of SS occur during biological treatment. Proteobacteria and Bacteroidetes were the most abundant in aerobic and anaerobic conditions, respectively [67, 68]. As reported by Rimkus et al. [47], addition of three types of carbon sources (faba bean straw, wheat straw, and wood-chip pellets) to the raw SS resulted in considerable changes in microbial community structure after 16 days of aerobic incubation. In particular, abundance of Firmicutes increased from 5% in the raw SS to 35–50% in the treated samples. In turn, abundance of Proteobacteria decreased from 62% in the raw SS to 32–45% in the treated samples. Yet, the SS incubation without C amendment resulted in a remarkable increase in virus abundance (i.e., 0.34% reads) [47]. The relative abundance of Salmonella enterica and Escherichia coli has been increased in the treated sludges, as compared to the raw SS (Figure 5B).

6.2 Shift in soil microbial community structure after application of the sludge-derived fertilizer

When SS is applied to soil, it causes changes in the structure and functioning of the agroecosystem. The most sensitive component is the soil microbiota, which can undergo both stimulatory and inhibitory changes in the activity and structure. These changes are greatly dependent on soil characteristics and SS application rate.

The microcosm experiment with SS-amended sandy soil (25.71 g SS/kg dry soil) after 119 days has revealed significant changes in prokaryotic community composition at the phylum level, as compared to the non-amended control [48]. Specifically, in SS-amended soil, the relative abundance of Firmicutes reduced from 58.6% at Day 0 to 18.7% at Day 119, while Proteobacteria increased from 15.5% to 36.4%, respectively [69]. In the control soil, these two respective phyla did not change considerably for 119 days. The relative abundance of Actinobacteria in SS-amended soil has increased from 3.1% to 13.2%, while in the control soil decreased from 27.6% to 19.4% [69].

The use of sludge as a soil amendment has been shown to increase the activity of soil enzymes, for example, arylsulfatase, acid phosphatase, and alkaline phosphatase. Basal respiration and the fluorescein diacetate hydrolysis activity increased with increasing the dose of SS [70]. Changes in urease activity by soil microorganisms can be discussed in two aspects. First, urease activity reflects the activity of microorganisms involved in the nitrogen cycle in soil [71]. Another aspect is related to the global loss of nitrogen (up to 70%) due to urease activity if urea is applied as a fertilizer. Therefore, urease inhibition is one of the strategies worldwide to maintain soil fertility [72]. In our experiments, combination of dry SS with nitrogen-containing fertilizer resulted in inhibition of urease activity in loamy soil during the vegetation experiment with maize [73].

The addition of SS-derived organics to soil increases the C_mic/C_total and N_mic/N_total ratios in the soil. At the same time, application of SS containing heavy metals, according to Fließbach et al. [8] and Chander and Brookes [74], C_mic/C_total ratio decreases to 32% and 50%, respectively. This effect can be developed greater in sandy soil than in clayey soils [75].

6.3 Indicators of microbiological contamination

In the early nineteenth century, the total coliforms, fecal coliforms, and fecal streptococci were considered as typical indicator bacteria. Later it was shown that these pathogens are not a major concern in solid waste landfills or leachate [62, 76]. Nowadays, different types of bacteria (fecal coliforms and Escherichia coli, Salmonella, Shigella, Vibrio cholerae); diverse parasite cysts and eggs (Balantidium coli, Entamoeba histolytica, and Giardia lamblia, helminths); viruses (human adenoviruses, enteroviruses (e.g., polioviruses), diarrhea-causing viruses (e.g., rotavirus), hepatitis-A virus and reoviruses) and fungi are monitored as biological contaminants of SS. Depending on the type and amount, they can all be harmful to the environment and human health [62, 76].

7. Effect of sludge-derived fertilizers on the plant growth

Soil amendment with SS is useful for enhancing crop production, as well as the accumulation of nutrients and organic matter in the soil. However, the accumulation of humic substances (HS) in soil and plant tissues must be regularly observed in case the SS is continuously used [14]. The SS can be used as fertilizers also after pyrolysis [77]. Both sole application of SS and their respective biochars provided enough P for the plants to achieve biomass higher than conventional P-fertilizer [77].

The effect of SS on plant growth differs depending on the SS application method, that is, at the soil surface “mulching” or mixed homogeneously with soil. The application of SS on the surface has some advantages, that is, water evaporation is limited by forming a physical barrier that allows soil moisture to be retained longer. Due to those, the biological and chemical processes of organic matter transformation intensified [78]. For example, the best yield of wheat (Triticum durum Desf.) was obtained when SS (dried) is applied at the clayey-silty soil surface (mulching) as compared to homogeneously mixed SS with soil [78]. Plant response to SS in dependence on SS application rate, plant species, soil type, and experiment conditions is shown in Table 1.

Importantly, a direct application of SS on agricultural soils is not recommended. It was shown that the hygienically treated (by liming) SS inhibited the growth of white mustard (Sinapis alba L.) already at a ratio of 10%. The addition of compost (5%, 15%, and 25%) resulted in the suppressed phytotoxicity of sludge in all tested ratios, that is, from 5 to 50% [92].

Our experiments showed that the use of SS affects the germination and development of seedlings. Concentrations exceeding 7 g kg⁻¹ inhibited the germination of cucumber seeds and resulted in necrotizing primary roots. In the study with air-dried SS mixed with agricultural sandy loam soil at rates of 0 (control), 10, 20, 30, 40, and 50 g kg⁻¹ (equal to 0, 30, 60, 90, 120, and 150 t ha⁻¹), seed germination of broad beans (Faba sativa Bernh.) decreased from 70.0% (control), to 63.3, 56.7, 50.0, 50.0 and 46.7%, respectively [14]. Nevertheless, all the growth and morphometric parameters of broad beans positively respond to SS-amended soil compared to non-amended soil. The most effective for biomass yield of broad beans was the application of 120 t ha⁻¹ SS [14]. In experiments with barley, the stimulation effect of SS also was shown, particularly, the addition of SS 40 g kg⁻¹ soil led to an increase of dry weight, leaf area, number of leaves, and tillers per plant [18].

Our recent study demonstrated a positive effect of SS on maize growth and soil microbiological activity, when SS is applied in combination with mineral fertilizers [73]. Additional experiments have been performed also with cucumbers and leaf mustard. The SS preparation alone did not provide the plants with mineral nutrients in appropriate values, while the combination of SS preparation with nitrogen-containing fertilizers significantly improved the plant growth and promoted plant development [73] (Figure 6). This may have a long-term favorable effect on plant mineral nutrition. Our data also showed that different plants respond to the SS differently. A species-specific effect, in that case, can be explained by (i) different sensitivity of plants to the compounds in SS preparations; (ii) demand for mineral elements at the early stages of ontogenesis due to slow release of nutrients from SS; (iii) insufficient maturing and the presence of growth inhibitors in SS.

Figure 6.

The effect of SSP on the growth of plants: A—cucumbers, B—leaf mustard, C–E—maize. Label color: pink—SSP + NPK, orange—NPK, blue—SSP + PK, green—SSP, yellow—vermicompost, white—soil without fertilizers. SSP—sewage sludge preparation; PK—phosphorus and potassium-containing fertilizer; NPK—nitrogen, phosphorus, and potassium-containing fertilizer. Controls—loamy soil without additional fertilizer, soil mixed with mineral fertilizer (Kristalon 18:18:18). Period of vegetation experiment A—18 days, B—47 days, C—33 days, E—46 days, and D—62 days. The application rate of SSP is 17.3 g L⁻¹ in a loamy soil. Methods are according to Dubova et al. [73].

8. Environmental impact of the sewage sludge

Sludge production globally in 2017 was 45 MT by dry matter, and now it is increasing annually due to urbanization and population growth [34, 93]. In this respect, the environmental impact of SS in the case of landfill disposal, agricultural use, or other applications is of great importance. Particularly, the contribution of different processes of SS treatment for agricultural use is recently studied by [59]. Energy consumption for SS treatment contributed mostly to global warming (>50%), while SS transportation to agricultural areas affected terrestrial and freshwater ecotoxicity, as well as ozone formation—terrestrial ecosystems (Figure 7AandB). Sludge disposal in agricultural areas mostly contributed to human toxicity, terrestrial acidification, and freshwater ecotoxicity (Figure 7C). The main impacts of SS in soil are related to the presence of Zn, which affects freshwater ecotoxicity and human toxicity [94].

Figure 7.

Environmental life-cycle assessment of the sewage treatment plant: contribution of different activities. A—energy consumption; B—transport of sludge to agricultural areas; C—agricultural areas sludge disposal. By Do Amaral et al. [94].

Biogeochemical emissions from SS handling and spreading on land are expected to be minimized in the future by efficient utilization of nutrients and other resources derived from SS, according to the principles of a circular economy [95, 96]. The processed land-applied SS can emit volatile chemicals and gases that may act alone or in combination with one another to produce the kinds of symptoms [63].

The composition of the sludge and the concentration of pollutants in it predetermine the possibilities of its use. The presence of heavy metals, organic pollutants, and/or pathogens are the main issues associated with the reuse of SS or biosolids extracted from it. According to Manzetti and van der Spoel [97], the following aspects can be reported—(a) raising of the levels of persistent toxins in soil, vegetation, and wildlife, (b) potentially slow and long-termed biodiversity reduction through the fertilizing nutrient pollution operating on the vegetation, (c) greenhouse gas emissions, and (d) the release of odorous compounds. Groundwater contamination from biosolids with pathogenic microorganisms is one of the greatest problems worldwide, due to the lack of adequate and equitable sanitation of SS [98]. Chemical contaminants in processed SS may potentially interact with microbial pathogens, thus, causing or facilitating the disease process via allergic and nonallergic mechanisms, as well as microbial byproducts [63]. Furthermore, endotoxins and exotoxins, which are produced by most bacteria in SS and retain their toxicity at extremely high dilutions, can cause severe illness or death. Endotoxins are heat stable even upon autoclaving, while can be inactivated with dry heat at temperature above 200°C for 1 h [79, 99, 100]. A high microbial diversity of SS leads to the horizontal gene transfer and proliferation of antimicrobial resistance (AMR) [101]. The virus persistence in SS is dependent on the physicochemical and biological properties. For example, enveloped viruses survive for 6–7 days in SS [102], while SARS-CoV-2 might persist on the surfaces up to 72 h [69]. Coronavirus can persist in domestic and hospital SS also for a longer period of time at lower temperatures (4°C) [62, 103].

Long-term accumulation of toxic elements in soil and their uptake by plants is currently the biggest concern in terms of direct SS land application. The bioavailability of heavy metals in the soil is closely related to the value of the soil exchange reaction (soil pH measured in KCl or CaCl₂ form), as well as to the sorption properties of the soil, which change with the addition of SS. According to published data, the availability of heavy metals in soils decreases in the order (Zn + Cd) > (Ni + Cu) > (Pb + Cr). However, in connection with physicochemical processes, the accumulation of heavy metals may occur over time, so it is necessary to monitor their concentration for a long time after the application of sludge [104]. When sludge is incorporated into the soil, the heavy metals in it bind to organic matter and clay particles, which usually accumulate in the soil [8, 105].

In Latvia, no more than 14 t ha⁻¹ of dry matter may be incorporated at a time with sludge or compost. This corresponds to 55 t ha⁻¹ of naturally moist sludge with a dry matter content of about 25% [106]. For 18 years, the concentration of heavy metals in Jelgava SS has significantly decreased. Similar trends have been observed in other treatment plants and this shows that heavy metals are no longer the most important limiting factor for the use of SS.

Wastewater can transport plastics from many different sources, such as fibers from washing machines, personal care products, and facial scrubs. WWTP efficiently removes the microplastics (MPs) from the wastewater, essentially trapping the particles in the sludge [107, 108]. Studies of Peterson [76] showed that 9 years of repeated sludge application led to the accumulation of MPs in the soil. According to various studies, MPs pose various negative effects on soil ecosystems, such as affecting soil fertility, soil organisms’ fitness, soil texture, and decreasing crop yield [109, 110].

Pignattelli et al. [111] highlighted the toxicity caused by small MPs (PP, PE, and PVC) on the growth of garden cress (Lepidium sativum). Hernández-Arenas et al. [112] studied the effect of MPs in sludge on the growth of tomato plants and discovered that plants grown in soils treated with sludge with a high concentration of MPs had the lowest biomass and did not produce any fruits during the experiment.

Domestic SS is a major source of pharmaceuticals, drugs, and antibiotic resistance genes, so it is important to ensure its biodegradation during sludge treatment. Drugs can remain in the sludge even after stabilization (dewatering), due to their high sorption capacity [113]. Ivanová et al. [114] discovered more than 100 types of drugs and their metabolites in SS. The amount and type of antibiotics in wastewater affect also the composition of bacteria [115].

Pharmaceutical substances are subject to thermal decomposition over a wide temperature range; therefore, it is possible to expect a reduction in the content or their complete removal during thermal processes [116]. Szabová et al. [117] achieved almost 100% drug removal in the sludge by heat treatment at 250°C and incineration at 550°C. Furthermore, pyrolysis at 350–500°C is able to decrease the concentration of MPs in sludge by more than 99% [118].

9. Future direction, challenges, and scope of sewage sludge as a soil fertilizer

The efficient use of waste-derived fertilizers in agriculture needs more empirical knowledge on markets with further research focused on variability, interactivity, and uncertainty. The site-specific factors (e.g., applied technology, quantity, and the origin of raw wastewater differed by the composition of macro- and microelements and risk compounds, soil types, and crops) make each SS unique, hence this specificity must be considered to predict the outcome of SS treatment. New efficient technologies for onsite sludge disinfection are necessary and urgent. Interdisciplinary activities on the safe use of SS upon treatment and application need to be thoroughly analyzed and developed, for example, planning, servicing, diagnosing, storing, and others. Furthermore, macroeconomic factors can considerably influence technology stocks. Soaring gas prices directly affected the production of synthetic fertilizers costs. High prices as well as the disruption of transport and production logistics lead to a real threat of a dramatic reduction in supply on the mineral fertilizers market. Combined with higher prices, an increase in demand for less volatile organic fertilizers can be expected.

10. Conclusions

Summarizing our experimental data on optimization of SS treatment and its application in agriculture, as well as recent findings of other authors in this field, the following conclusions were drawn:

The technology, which was newly developed by Earth Revival Ltd., offers an innovative and comprehensive solution to the problem of SS disposal and soil degradation, which includes aspects of agriculture, healthcare, epidemics, ecology, economics, and the social sphere. Costs can be recuperated through sludge treatment service fees and fertilizer sales.

The infrared heating system, used for SS disinfection, has shown consistently successful results. For the material with a humidity of 80%, it took 15 min, considering the heating time of the layer to 95°C, which is below the temperature of the organic matter decomposition. Research and experiments related to the neutralization of the spore-forming bacteria are planned to be realized in the next stage of the project.

The technology (SS transportation system, maturation process) can be used for fast, safe, and efficient SS processing into organic fertilizer. It also combines well with the anaerobic digestion process as it can complete the digestive sludge transformation to a huge quality fertilizer.

Sewage sludge can replace mineral fertilizers in crop production. Attention should be paid to the amount and ratio of mineral elements available to the plant during plant growth. Sewage sludge may not fully provide plants with potassium and phosphorus. Sewage sludge is recommended for plants with a longer vegetation period due to the slow release of nutrients. A phytotoxic effect may occur during seed germination.

Acknowledgments

This research is being conducted based on agreement with SIA “ETKC” (Centre of Competence for Energy and Transportation) within the framework of project Nr.1.2.1.1/18/A/001 co-funded by the European Regional Development Fund.

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.