A review on the fate and effects of contaminants in biosolids applied on land: Hazards and government regulatory policies

Abstract

The increase in world population growth and its resultant increase in industrial production to meet its need, have continued to raise the volume of wastewater received by treatment plant facilities. This has expectedly, led to an upsurge in the volume of sewage sludge and biosolids generated from wastewater treatment systems. Biosolids are best managed by application on land because of their agronomic benefits. However, this usage has been discovered to negatively affect humans and impact the environment due to the accumulation of minute concentrations of contaminants still present in the biosolid after treatment, hence the need for government regulations. This review article examined the fate and effects of pollutants, especially persistent organic pollutants (PoPs) of concern and emerging contaminants found in biosolids used for land applications, and also discussed government regulations on biosolid reuse from the perspectives of the two major regulations governing biosolid land application-the EU's Sludge Directive and USEPA's Part 503 Rule, in an attempt to draw attention to their outdated contents since enactment, as they do not currently meet the challenges of biosolid land application and thus, require a comprehensive update. Any update efforts should focus on USEPA's Part 503 Rule, which is less stringent on the allowable concentration of biosolid pollutants. Furthermore, an update should include specific regulations on new and emerging contaminants and persistent organic pollutants (PoPs) such as microplastics, pharmaceutical and personal care products (P&PCPs), surfactants, endocrine-disrupting chemicals, flame retardants, pathogens, and organic pollutants; further reduction of heavy metal standard limits, and consideration of soil phosphate-metal interactions to regulate biosolid agronomic loading rate. Future biosolid research should focus on the concentration of TCS, TCC, and emerging pharmaceuticals, as well as Microplastic transport in biosolid-amended soils, soil-plant transfer mechanism, and metabolism of PFAs in the soils; all of which will inform government policies on biosolid application on land.

1. Introduction

The proliferation of industries, urbanization, and industrialization of suburbs and rural areas over the past decades around the world, has resulted in an increased standard of living [[1], [2], [3]] together with its attendant increase in the volume of wastes generated, especially sewage and industrial wastewater [[4], [5], [6], [7]] (with Asia generating highest volume according to a projection of global wastewater generation, Fig. 1), which has to be treated before discharged into the environment to prevent pollution [8,9]. According to Giacomo and Romano [10], municipal wastewater generated in the world in 2020 was between 360 and 380 cubic kilometers, which is a projection of a 24% and 51% increase by 2030 and 2050 respectively.

Fig. 1.

Projected increase in global wastewater generation since 2015 [11].

Wastewater treatment generates sewage sludge and effluent as end products [10,12,13]. Due to an increase in wastewater production as a result of population growth in the last couple of years [14], there has been a corresponding increase in sewage sludge production [[15], [16], [17]]. According to Collivignarelli and Abba et al. [18], the total sludge production from urban wastewater plants in the EU-15 countries has increased from 6.5 MT (dry weight) to 9.5 MT (dry weight) over the last two decades and, EU-27 countries saw sludge produced up to 10 MT (dry weight) during the same period; the yearly per capita sludge generation in Europe in kg dry matter per inhabitant per year (kg DM/inhabitant year) is shown in Fig. 2 which revealed that Portugal and Italy both members of EU-15 countries, had the highest and lowest sludge generation per inhabitant respectively. Chow and Pan [19], gave the total sewage sludge produced per day from different treatment plants in Hong Kong as 1200 tons and, this figure is projected to reach 2000 tons by 2030 as a result of the improvement of treatment plant operations [20,21], environmental discharge standard [22] and population increase [10,20,23].

Fig. 2.

Comparison of yearly sewage sludge generation per person in Europe [24].

Raw sewage sludge contains a high level of contaminants whose concentration has to be reduced by subjecting sludge to further treatment or processing before useful applications [[25], [26], [27]]. Land application of raw sludge is restricted because it can result in severe environmental risks [[28], [29], [30]] such as water pollution and soil contamination due to the presence of heavy metals including Chromium (Cr), Copper (Cu), Nickel (Ni), Zinc (Zn),Lead (Pb), Cadmium (Cd) [31,32],Ethers (PBDEs), Di(2-Ethylhexyl) Phthalate (DEHP), Polychlorinated Biphenyls (PCBs), Polycyclic Aromatic Hydrocarbons (PAHs), Polychlorinated Dibenzo-p-dioxins and Dibenzo-p-furans (PCDD/Fs) [33,34], pharmaceuticals, endogenous hormones, synthetic steroids [35] and, organic, antimicrobial pollutants known as Per- and Poly-fluoroakyl substances (PFAs) [36,37]which can all accumulate in soil or washed to surface water during any short or long term sludge use [38,39].

2. Sewage sludge treatment technologies

The large quantities of sewage sludge produced at water treatment plant facilities undergo certain treatment processes to convert it to biosolid (Fig. 3) for more beneficial use. Major reasons for the treatment of sewage sludge are to drastically reduce the amount of disease-causing pathogens and contaminants [40], reduce the volume of sludge for better handling [41], make sludge economically more viable [42], and to reduce the attraction of vectors such as flies, fleas, rodents, mosquitoes, birds; all these are referred to as vectors in the EPA's Biosolid Rule [43]. Some of these treatment technologies, which include anaerobic sludge digestion, incineration, sludge compost, sludge drying, deep-dewatering/thermal hydrolysis, and alkaline stabilization/pH treatment [19], are discussed below.

Fig. 3.

Block flow diagram showing biosolid production from wastewater treatment [49].

2.1. Anaerobic sludge digestion

This sludge stabilization process involves the use of biological microorganisms in the absence of air to convert volatile solids in raw sewage sludge to biogas, carbon dioxide, and water [44]. The biogas produced during this process can be further treated for energy recovery to utilize its methane component as fuel while the stabilized solids (biosolids) can be used for soil conditioning [44]. Anaerobic sludge digestion is the most commonly employed sludge stabilization process and unlike aerobic digestion, it is lower in energy utilization and generates fewer wastes; it also uses fewer chemicals than alkaline stabilization. However, it has a higher initial capital cost and complex operation than the other processes [44].

2.2. Sludge incineration

Incineration of sewage sludge is a thermal treatment process [45] that oxidizes organic sulphur, nitrogen, carbon, and phosphorus in raw sludge to inorganic, mineral solid, and gaseous products [44]. The process may be carried out in a furnace at a high temperature greater than 800 °C so that the organics in sewage sludge may be oxidized [45].

2.3. Sludge composting

This is an aerobic sludge digestion process that uses biological thermophilic or mesophilic microorganisms in the presence of air, to degrade raw sewage sludge combined with other waste materials such as rice hulls, straws, sawdust, and recycled compost (amendments) and, shredded green wastes, tyres, and wood scrapes (bulking agents) to produce a pasteurized solid product [44]. The stages involved in sludge composting include 1). Mixing raw sludge with amendments or bulking agents at the preprocessing stage, 2). Aerating the mixture for decomposition using air provided by a mechanical pumping device, 3). Recovery of undegraded additives (amendments and bulking agents), 4). Stabilizing the product formed by curing and storing and, 5). Screening, grinding, or comminution to remove undegraded materials and produce a uniform product [44].

2.4. Sludge drying

This is an intermediate thermal intervention process for treating wet sewage sludge that involves reducing/evaporating the moisture content of raw sludge thus, significantly lowering its weight and volume for better handling and recovery to meet important applications such as its use as fuel for incineration plants, compost material, and fertilizer [46].

2.5. Deep-dewatering/thermal hydrolysis

Raw sewage sludge can be treated by first subjecting the sludge to a deep-dewatering process before thermal hydrolysis. Deep-dewatering, which involves removing moisture from sludge to reduce its overall volume for better operational handling and subsequent cost of transportation [47], is carried out to thicken sludge to about 16–18% of dry weight [48]. The partially thickened sludge is then exposed to high temperature, between 160 and 180 °C, and a pressure of about 6 bars in the thermal hydrolysis step to sterilize the sludge and kill pathogens [48].

2.6. Alkaline stabilization/pH treatment

This is a chemical treatment method employed to reduce pathogenic colony, putrescence or decay, and odour during the sludge treatment process. It involves the use of slaked or hydrated lime (calcium hydroxide) to raise the pH of raw sludge to create a high alkaline system [44]. The amount of lime used may be reduced by dosing waste solid materials into the system thereby making the system cost-efficient [44].

3. Biosolid management and disposal methods

Biosolid management technologies are employed to dispose of the large quantities of biosolids generated from sewage sludge treatment. Many researchers have described biosolids as treated sewage sludge materials produced to meet Environmental Protection Agency (EPA) standards for agriculture and land application [12,36,43,50,51]. Kinney and Furlong et al. [52] in their study, defined biosolids as carbon-rich, organic beneficial solids, produced during wastewater treatment to meet local and United States Environmental Protection Agency (USEPA) regulations for pathogen, metal, and nutrient content, suitable for land application and, Thomas Burke [13], noted that biosolids are the main organic solids from municipal wastewater treatment that can be valuably recycled to amend agricultural soil.

Biosolid scan be classified as class A or class B solids and this classification is based on sewage sludge treatment methods [53] and the extent of pathogen reduction [13,43,54]. Class A biosolids are produced when sewage sludge is treated so that the presence of pathogens is below the detectable amount [27]. It can be bagged, sold to the public, and used without restrictions based on its pathogen content [43,53]. Class B biosolids, on the other hand, are produced when sewage sludge is treated to only reduce pathogen concentration which may still be detectable [27]. They are regulated for use on land to prevent man and animal exposure to contaminants, or environmental degradation [43,53].

Biosolid management and disposal techniques have evolved over the years with many countries favouring land/agricultural application to incineration, landfilling/surface disposal, or production of building materials, etc. [55]. In the United States for instance, of the 8.2 million tons of biosolid produced in 2010, 54% were land applied compared to 18% and 19% that were landfilled (surface-applied) and incinerated respectively (Fig. 4) [56]. In the same vein, the United Kingdom Water Industry Research (UKWIR) [50], noted that 150,000 ha of agricultural land in the U.K. utilized a total, between 3 and 4 million tons of biosolids produced annually for land application, representing more than 75% of the total production quantity compared to other sludge management practices including incineration/energy recovery which utilized 12% of total sludge produced, land reclamation 5%, and others 5% (Fig. 5) while, in China, approximately 39.04 million tons of biosolids were produced annually (2019 data) from which 29.3% was disposed via land application, 26.7% incinerated, and 20.1% landfilled [57]. Some of the disposal routes of biosolids currently in use include land application, incineration, sanitary landfilling/surface disposal, and production of construction materials [51,57] are discussed in the following section.

Fig. 4.

Biosolid management and disposal practice in the U.S [5].

Fig. 5.

The UK biosolid disposal pathways [50].

The pie diagrams shown above (Fig. 4, Fig. 5), clearly revealed that land application of biosolids is the most popular/common biosolid management practice in the U.S. and UK.

3.1. Land application

Biosolid land application involves spreading the stabilized, treated solids on surface soil or incorporating them into the ground on the basis of government regulations and guidelines [5]. This practice can occur at sites such as forests, mine reclamation sites, agricultural lands, disturbed lands, golf courses, or parks [5]. Land application of biosolid is sustainable, cost-effective, unlikely to cause environmental degradation, and generally improves soil fertility making it a widely accepted technique in many regions [50,56,57].

3.2. Biosolid incineration

Biosolid incineration is an “end-of-useful-life” approach to biosolid management. This is because after subjecting biosolid to high-temperature combustion in the presence of air and converting it to carbon, ash, and char, it is taken to a landfill site for surface disposal [57]. Incinerating biosolids before landfilling kills and inactivates pathogens that could cause environmental pollution [56]. Incineration as a biosolid management technique is discouraged as a result of the release of toxic, greenhouse gases into the environment thereby, causing air pollution [57].

3.3. Sanitary landfilling/surface disposal

The biosolid landfilling/surface disposal management option involves dumping biosolids in excavated spaces and then compacting and leveling the area to reduce waste volume [58]. The disposal can be on a mono-disposal landfill where only solid wastes from wastewater treatment are dumped; this type of landfill is regulated by the 40 CFR Part 503 legislation or, on a mixed landfill (co-disposal landfill) where biosolid wastes are combined with municipal solid wastes (MSWs), which is regulated by the 40 CFR Part 258 legislation for MSWs [5,56]. Management of biosolids by landfilling should be distinguished from land application practice, where biosolids are applied to soil for enhancements [56]. It is important to point out that landfilling biosolids can result in severe public and environmental health complications due to the uncontrolled release of contaminants into the environment [56].

3.4. Production of construction materials

Application of biosolids in the field of construction is one of the sustainable disposal routes of biosolids, which is dependent on the material's geotechnical properties. Modified/stabilized biosolid composites and aggregates applied in construction can be used for embankment filling, land reclamation, brick manufacture, and the development of other construction materials [49]. Biosolid's use in this way is a major contribution to the circular economy ecosystem. The addition of substances like lime, cement, bauxson, glass, and fly ash has been reported to greatly enhance the stability, compaction characteristics, shear, and compressive strengths of biosolids [49]. Usually, before composites are applied in construction, standard tests such as large-scale direct shear tests, vane shear tests, cone penetration tests, triaxial tests, California bearing ratio, consolidation tests, compaction tests, etc. [49].

The present review article adopted the narrative research design to provide a contributory insight into the evidence of environmental hazards associated with biosolid land application disposal routes and discussed government legislations that regulate this biosolid management technique including how application practices can influence government policies. A flowchart of the research concept is shown in Fig. 6A scoping search was initially carried out to identify the knowledge gap in the field and develop a research question. Using keywords and phrases in the research question, which are combined with Boolean operators, an elaborate search for literature in major databases such as Scopus, Google Scholar, and Science-Direct was done. The total number of relevant articles obtained after applying inclusion/exclusion criteria such as year of publication, title, originality of the study, whether the study was peer reviewed or not, methodology, and reported outcome or conclusion, was 150. These articles were each assessed for limitation and bias using the Cochrane Collaboration Tool with a low overall risk of bias.

Fig. 6.

Flow chart of research concept.

4. Biosolid land application and the circular economy

The need for land or agricultural soil amendment especially in an arid or semi-arid region where crop yields are very low, as a result of the combined effects of harsh climatic conditions like land degradation occasioned by erosion, long and persistent drought conditions, poor cultivation practices, etc. [59,60], has necessitated biosolid application practices on land for agricultural purposes [61]. This practice of recycling biosolids as organic fertilizer on land is an aspect of the circular economy [62] that tends to eliminate large volumes of sewage sludge produced annually around the world, especially in the developed world, and thus, reduce its environmental pollution by reprocessing and consuming it, forming a circle of sludge regenerative production and consumption [63].

Being a widely practiced and economically viable biosolid management method, biosolid land application in agriculture as soil amender and conditioner [12] has been reported to enhance the diversity of soil beneficial bacteria (rhizosphere bacteria) community, plant performance, and growth, improve soil properties [64], provide nutrient and stable organic matter to soil [12,50,65]. The organic nature of biosolids makes them better alternatives to mineral (inorganic) fertilizers [61] as they are high in plant nutrients such as nitrogen, potassium, phosphorus, organic matter and, can improve the yield and quality of crops [12]. Also, biosolids’ slow-release of plant nutrients (which may potentially reduce pollution caused by leaching of excess nutrients, a common occurrence with mineral fertilizer)make them readily available to plants and increase their efficiency for plant growth and soil enhancement; these and together with their low cost make them more attractive than mineral fertilizer [12,54,66].

4.1. Biosolid land application best practices

Recycling biosolids to agricultural soils, rangelands, forests, and damaged lands to replenish soil organic matter, supply soil nutrients, and enhance land reclamation is known as biosolid land application [66]. Such land application has been observed to increase plant drought tolerance and improve soil texture and water holding capacity [67], which favour root and shoot growth and, remediate disturbed land area [66]. Application of biosolids on land, however, can result in environmental pollution due to the bioaccumulation of excess nutrients from repeated use as organic fertilizer [68]. It is therefore important to apply biosolids while observing certain management practices (Best Management Practices) which can allow for proper usage and protection of human and environmental health [54].

• (a)Following Strict Biosolid Agronomic Loading Rate: This describes the frequency at which solid or liquid biosolid is applied (or injected) to an agricultural area of known dimension [69,70]. High loading rates may result in the accumulation of nutrients like phosphorus on soil surfaces thereby, increasing the likelihood of runoff (caused by erosion) to streams causing water pollution [54]. The application rate of biosolids should be determined by soil nitrogen requirement if the phosphorus index of the soil is low or medium and, by reducing phosphorus content if the index is high [54]. Application rate should also consider soil nutrient content and crop requirement (by considering trace element content of the soil) as well as, nutrient content of the biosolid (considering trace elements content of the biosolid) [54].
• (b)Application Site Slope Limitation: Biosolid land application should consider site steepness or slope to avoid excess nutrient runoff to nearby plateaus or streams [70]. Usually, for sites with 0–6 unit slopes, the application rate is not limited but may be varied when erosion is a concern and soil conservation practices are employed on sites with 7–12 unit slopes [71]. Biosolids can be applied on grass vegetation sites with more than 80% of the site covered, for slopes of 12 units and above [71].
• (c)Application Site pH Limitation: The availability of soil nutrients for plant growth is affected by soil pH value [72]. Depending on the soil solution pH test (whether salt or water solution test) conducted, biosolid application on sites should be avoided when pH is within the acidic region of less than 6.0 or alkaline region of greater than 7.5 for a salt test or, 6.5 and 8.5 for a water test [71].
• (d)Establishing Buffer Zones: Biosolid application is discouraged on neutral land areas around natural water bodies like sink boreholes, ponds, wells, etc., for environmental protection [73]. These buffer zones (neutral areas) can be established about 300 feet from water bodies, 150 feet from residential areas or dwellings, 100 feet from wetlands, and 50 feet from intermittent flowing streams [71].
• (e)Restriction of Public Access to Biosolids: General public use of biosolids should depend on the type and government approval for public use. Class A biosolids to be applied on home gardens, root and vegetable crops gardens, and other public sites must comply with strict regulations and must be approved by the government before distribution or use [71,74]. Class B biosolids should not be applied on public sites, turf lawns, or residential farms, unless they are produced by a regulated industry (i.e. incorporated) [71].
• (f)Encouraging Biosolid Application Deferment on Grazing Land: Biosolid land application should be discouraged immediately after livestock grazing or crop harvesting on agricultural fields to prevent pollution caused by nutrient washout (run-off) which may occur after these activities as the soil becomes prone to erosion [69,70]. Generally, a 30-day period should be allowed before biosolid application on land after grazing or harvesting [69].
• (g)Encouraging Soil Conservation via Biosolid Application: Biosolid application on land can protect topsoil from erosion and maintain soil productivity and fertility [75], as the organic matter present in biosolid help to increase soil water holding capacity, reduce compaction [67,76], and provide a platform for microbial activity [71].
• (h)Discouraging Biosolid Application on Saturated or Frozen Soil: Biosolid land application should be discouraged on frozen, snow-covered, or saturated soil unless restriction controls can be employed to prevent pollution from snowmelt or water runoff [71]. If biosolid must be applied on frozen soil, then the land must have a maximum of 2 or 6 units of slope and a buffer area of 100 or 300 feet respectively and must be allowed between a water body and the application site [71,77,78].
• (i)Protection of Threatened Biological Species: Biosolid land application should be practiced in such a way that it does not harm endangered soil biota such as bacteria, fungi, earthworms, protozoa, nematodes [71,79], insects [69] or, threaten their habitat [80].

5. Fate, environmental hazard, and effects of contaminants in Biosolid applied on land

Although biosolids are beneficial to crops when used as organic fertilizer and soil conditioner [81], they do contain contaminants at minute concentrations in nanogram/liter (ng/L) or lower (the concentrations of contaminants in biosolids are usually below regulatory standards), which can accumulate in soils [82] due to repeated land application and, eventually cause environmental pollution [83]. These emerging contaminants discovered in biosolids may include pharmaceuticals and personal care products (P&PCPs) such as prescription drugs that may be found in human faeces and urine [84,85] and, chemicals in soaps, detergents, shampoo, etc. [83], endocrine-disrupting chemicals (EDCs), surfactants, flame retardants, per-and poly-fluoroalkyl substances (PFAS) [84], microplastics (or nanoparticles) in toothpaste and laundry wastewater, etc. [[86], [87], [88]], which all enter the wastewater treatment plant and thus, sewage sludge through the sewer system, remaining in biosolid after sludge treatment as treatment does not completely remove these contaminants [27]. When contaminants enter the environment through biosolid application on land, they may be persistent, degraded, undergo additional transformations, or converted into by-products with hazardous effects on the environment [84].

Researchers have studied the effects and potential hazards of biosolid contaminants on the cell structure, reproduction, biochemistry, growth, and mortality of the flora and fauna colony in an environmental ecosystem [89,90]. While some of the literature reviewed agreed that contaminants may have a minor effect at low soil accumulation on soil microbes and animals [89], others presented evidence of a major effect on terrestrial and aquatic animals [[91], [92], [93]]. For instance, Diclofenac, a pharmaceutical drug detected in soil amended with biosolid, was linked to a drastic decrease in the vulture population in Pakistan [91]. Also, Garric et al. [92] in their study, demonstrated the effect of Ivermectin on the development of aquatic invertebrates and Lange et al. [93] demonstrated the endocrine disruptive effect of Ethinylestradiol (a drug used for contraception in humans) in fishes. It is therefore imperative to understand the fate and hazardous effects of emerging contaminants and persistent organic pollutants (PoPs) found in biosolid used for land application in order to prevent environmental pollution and inform government regulations on biosolid use.

5.1. Heavy metals

Biosolid application on land may be limited by its heavy metals content [35]. Heavy metals such as arsenic (As), mercury (Hg), selenium (Se), molybdenum (Mo), titanium (Ti), antimony (Sb) [94], zinc (Zn), cadmium (Cd), copper (Cu), chromium (Cr),lead (Pb), and nickel (Ni) [95] are commonly found in biosolids and, their concentrations depend on the nature of wastewater and region of origination (Table 1) [96], wastewater treatment process [[96], [97], [98]], and the industrial manufacturing process [95]. Domestic or household wastewater usually has a lower heavy metal concentration than industrial wastewater [95]. While some heavy metals in biosolids are appropriate for plant growth at low concentrations (Mn, Zn, Cu), others (Pb, Cd, Hg, As) are not [99]. The accumulation of heavy metals in the soil becomes high over a long-term period of biosolid application and even, short-term use has been observed to raise their concentrations considerably [95].

Table 1.

Variation in concentrations of heavy metals in biosolids due to region and nature of wastewater generated.

Country	Zn	Cu	Cr	Pb	Ni	Cd	Hg
USA (1977)	1740.0	850.0	890.0	300.0	82.0	19.0	3.0
USA (2002)	750.0	511.0	35.0	65.0	23.0	2.3	1.5
France (1999)	761.0	286.0	4.5	107.0	35.0	4.5	2.1
France (2017)	60–200	20–100	30–100	70–100	15–70	0.5–1.5	0.1–1.0
China (2018)	674.0	204.0	236.0	26.0	334.0	0.9	0.9
Concentration limit, EPA (2002)	7500.0	4300.0	ND	840.0	420.0	85.0	57.0

ND = not determined. All values are in mg/kg [98].

5.2. Per- and poly-fluoroalkyl substances (PFAs)

These synthetic, organic chemical compounds, used in several applications such as water and heat-resistant fabrics [100,101], cleaning products, dental floss [102], shampoo, and cosmetics [103], paint production, industrial emulsifier and surfactant manufacture, non-sticky cookware, oil-repelling containers, aqueous film-forming foams for firefighting operations [84], etc., are found in sewage sludge and have been detected in soil amended with biosolids [36,104,105].

The number of PFA variants (Table 2) synthesized after the first (Polytetrafluoroethylene or PTFE) was produced in 1938, has been on a steady increase since the early 1950s and presently, there are over 5000 PFA compounds that have been commercially manufactured [106]. Of these PFA variants, long-chain PFAs such as polyfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) are most detected in polluted soils [107] as they are more persistent and bioaccumulative in the environment [36,106,108] due to their preferential bonding to the hydrophobic or protein binding site of the soil [106]. Because of the persistent fate of PFAs especially PFOA and PFOS in environmental matrices, their concentrations are elevated within a short period of biosolid application on agricultural soil [109,110] with the attendant phytotoxic effect on certain plant species [111]. This characteristic of PFAs has been demonstrated by researchers in various research, for instance, Damien [106], reported the phototoxic effect of PFOA on Thale Cress (used in genetic experiments) at a concentration in excess of 181 ng/L in a study to investigate the fate, behaviour, and ecological impact of biosolid-derived PFAs and, Li et al. [111], carried out a metabolomic study of Lettuce exposed to elevated concentrations of PFOS and PFOA, between 500 and 5000 ng/L and observed between 88 and 95 significantly disturbed metabolites (amino acids, prenol lipids, phenolic compounds, carboxylic acids)for PFOS and PFOA exposure respectively. Public health hazards of human and animal exposure to high levels of PFAs include reproductive defects, neurological development delays, low birth weight, bone variation, accelerated puberty, changes in liver and kidney functions, thyroid disease, testicular cancer, etc. [94,112].

Table 2.

Pollutants and emerging contaminants recently discovered in biosolid. Cl-PFCA: Chlorine substituted PFCA; UPLC-ESI-MS/MS: Ultra Performance liquid Chromatography with Mass Spectrometry and Positive Electrospray Ionization; PFHxS: Perfluorohexanesulfonic acid; ASE: Accelerated solvent extraction; PFHpA: Perfluoroheptanoic acid; PFEA: Perfluoroalkyl ether alcohol; H-PFCA: Hydro substituted PFCA; HPFSA: Hydro substituted PFSA; HPLC-FD: High performance liquid chromatography with fluorescence detection; LC-MS/MS: Liquid chromatography with mass spectrometry; LOD-limit of detection; FTS: Fluorinated telomer sulfonate; LOQ-limit of quantification; OBS: P-perfluorous nonenoxybenzenesulfonate; PFBS: Perfluorobutanesulfonic acid; Cl-PFESA: Chlorine substituted perfluoroalkyl ether sulfonate; GC/ECNI-MS: Gas chromatography/mass spectrometry operated in negative ionization mode; PFBA: Perfluorobutanoic acid; PFOS: Perfluorobutanesulfonic acid; PFOA: Perfluorooctanoic acid; PFPeA: Perfluoropentanoic acid; P&PCPs: Pharmaceutical and personal care products; PFSM: Perfluoroalkyl sulfonamide; SPE: Solid-phase extraction; UPFCA: Unsaturated PFCA; PFHxA: Perfluorohexanoicacid; HPFESA: Hydro substituted perfluoroalkyl ether sulfonate; PFAS: Poly & Per fluoroalkyl substances; UPFA: Unsaturated perfluoroalkyl alcohol [84].

In a study conducted by Oliveira et al. [113], the researchers reported that the concentration of Zn, Ni, Cr, and Cu in a biosolid-amended soil rose sharply over a relatively short period of two years. The speciation, bioavailability, and fate of heavy metals after biosolid application to the soil ecosystem is a function of the soil's (ionic strength, pH, and dissolved organic carbon) and biosolid's chemical characteristics [95]. Most metals are not biodegradable or chemically degradable and are, thus persistent in the environment [114,115] leading to metal leaching through soil profile and contamination of groundwater [99]. Heavy metals in the soil's rhizosphere (where toxicokinetic and toxicodynamic processes take place) in the form of dissolved free cations and negative, positive, or neutral species, are absorbed by plants through the root system [116], causing bioaccumulation of these metals [114]. Environmental effects related to heavy metal accumulation in the soil are severe on plants, animals, and humans alike [117]. Plant exposure to high concentrations of heavy metals may result in stunted growth, reduced yield, altered metabolism, etc. [116]. The effect of heavy metals on humans is the result of the biomagnification of these toxic chemicals in the body which affects different organs [118]. These effects on humans, which may be acute or chronic [118,119] include nervous system disorders, gastrointestinal and kidney dysfunction, immune system dysfunction, skin lesion, birth defect, vascular damage, and cancer [118].

5.3. Excess nutrients in biosolid

The major plant nutrients in biosolids are magnesium (Mg), nitrogen (N), potassium (K), phosphorus (P), sulphur (S), calcium (Ca), and micronutrients [120]. Among these nutrient types, P is commonly found in excess in biosolid-amended soils [121] because most of the phosphates in wastewater are retained in sewage sludge (biosolid)during the tertiary treatment step [122] and, because farmers by following government regulatory guidelines, apply biosolid to soil based on plant requirement of N, [121]; P accumulation in the soil thus increases rapidly as the ratio of N to P varies [123]. Long-term application of biosolid leads to excess concentration of P in top soils [121] which can be washed into surface water resulting in algae invasion and river eutrophication [123]. Increased phosphate concentration in the soil has also been observed to affect soil metal lability [124]. Mossa et al. [124], in a study, reported that with rising levels of metal concentration due to prolonged biosolid application, there is an interaction with increasing phosphate concentration, which reduces the lability of Pb and Cd metals and, increases lability of Zn, Ni, and Cu metals as a result of weak soil binding. These interactions between soil phosphate and heavy metal concentrations should be taken into account when the government sets regulatory standards [124].

5.4. Microplastics (MPs)

These emerging contaminants are plastic particles with diameters less than 5 mm [[86], [87], [88]]. MPs commonly found in biosolids include microbeads (Fig. 7) and microfibers (both primary MPs) manufactured by industries to act as fillers, abrasives [125], viscosity control agents [126], and for aesthetics purposes in fabrics, personal care products, consumer plastics [127,128], etc.; secondary MPs are formed by processes such as biodegradation, photo-oxidation, or mechanical abrasion of large plastic debris in the environment [129].

Fig. 7.

Microbeads used as abrasive in toothpaste [130].

Most MPs are collected in sewage sludge during wastewater treatment and are not completely removed when the sludge is treated to produce biosolids [86]. When MPs enter the environment through the application of biosolids on land, they are hardly removed (they can persist in the environment for many years) but can be fragmented into smaller-sized particles (nanoplastics have a size range less than 1 μm) by environmental forces [[86], [87], [88]]. MPs have been reported to act as vectors (carriers) for pollutants, heavy metals, hazardous additives, and pathogens, which can cause health complications in humans and animals [131]; these pollutants can be spread through contamination pathways such as water and food ingestion [132] as water and food samples have been discovered to contain them (e.g. salt, seafood, tap water, honey, and bottled water) [133].

5.5. Pharmaceuticals and personal care products (P&PCPs)

P&PCPs (structure of common pharmaceuticals in biosolids are shown in Fig. 8) are a wide range of manufactured products used for medical care and cosmetic purposes and, include substances like anti-inflammatory agents, steroidal hormones, antibiotics, detergents, perfumes and active ingredients in soaps [84]. Prescription drugs used by patients for the treatment of certain diseases are not fully absorbed by the body as remnants of these drugs and their metabolites, are passed out of the body during excretion into the sewer system [134,135]. From the sewer, the remnant drugs are transported to the wastewater treatment plant and then degraded by the secondary treatment process [136]. Most of the remnant drugs are trapped in the sewage sludge after wastewater treatment while a small concentration is contained in biosolid after sludge treatment [136].

Fig. 8.

Chemical structure of (a) acetaminophen (b) sulfadiazine (c) sulfapyridine (d) diclofenac (e) ibuprofen (f) atenolol (g) metoprolol (h) bezafibrate (i) clofibric acid (j) ethynylestradiol (k) gestodene (l) testosterone (m) fluoxetine (n) carbamazepine (o) caffeine and (p) cortisone which are commonly found pharmaceuticals in Biosolid [84].

The fate and persistence of pharmaceuticals in the soil following biosolid application depend on the drug's biodegradability [84], its physicochemical properties, and the molecular structure of its constituent chemicals but not on the soil's properties or bioactivity [137]. This persistence can affect plant uptake of, and bioaccumulation of these drugs which can determine their effect on humans as a result of ingestion [136]. For example, the pharmaceutical drug Carbamazepine was found to have a limit of quantitation (LOQ) as high as 52 μg/g and 33 μg/g in radish and ryegrass respectively, in a study to compare plants' uptake of pharmaceuticals in soil; whereas the LOQ for sulfamethazine was far lower at 0.01 μg/g in the same study [136]. The effects of bioaccumulation of Carbamazepine on plants include leaf chlorosis, tissue necrosis, inability to produce fruit, etc. [138]. Phototoxicity of Sulfamethazine at high levels in plants on the other hand causes root and stem elongation, root decay, necrosis, etc. [139]. In humans, the toxic effects of Carbamazepine trigger life-threatening allergic reactions such as Toxic Epidermal Necrolysis (TEN) and Stevens-Johnson syndrome (SJS), decrease the number of blood cells produced in the body, causing unusual bleeding in the gum, nose, heavy menstruation, shortness of breath, mouth sores, etc. [140]. Also, Sulfamethazine causes anaphylaxis, angioedema, and urticaria hypersensitive reactions in the human body and can result in skin rash, drug fever, agranulocytosis, polyarthritis, and hemolytic anemia, etc. [141]. Another effect of applying pharmaceutical-contaminated biosolids on agricultural land is the development of antibiotic-resistant bacteria or ARBs in the soil [136].

Triclocarban (Fig. 9a), Triclosan (Fig. 9b) and Triclocarban (Fig. 9c) are used as antibacterial ingredients in fast-moving consumer (FMCG) or personal care products that enter the wastewater treatment system from household wastewater (kitchen and bath wastewater) because of their use in liquid and bar soaps [142], are not completely eliminated from the sludge during wastewater treatment [143]. These chemicals also called 3, 4, 4′-trichlorocarbanilide and 2, 4, 4′-trichloro-2′-hydroxydiphenyl ether respectively, whose structure are shown in Fig. 9b and (c) respectively, have a low biodegradation potential and high persistence in the soil after biosolid application [[143], [144], [145]]; their degradation may increase with the amount of aeration available in the soil i.e. degradation rate is faster in aerobic than in anaerobic soil [144,145]. Negative effects of TCS and TCC in the environment can be seen in algae growth inhibition [146], fauna endocrine disruption [126], toxic or carcinogenic compound (such as chlorinated anilines, dioxins, and chloroform) formation on environmental biota, and chemical bioaccumulation especially in snails and earthworms [143].

Fig. 9.

Structure of (a) Triclocarban (b) Triclosan, and (c) Triclocarban [143].

5.6. Surfactants

These are organic chemicals often called surface-active agents because they help to reduce the surface tension of liquid media [84]. They are used for a wide range of applications including soap, detergent, dish cleaner and shampoo manufacture, production of lubricants and mining flocculates, and in wastewater treatment, textile industries, and petroleum recovery operations [84]. Commonly found surfactants in biosolid-amended soil are quaternary ammonium compounds, linear alkyl benzene sulfonates, alkyl ethoxylate, alkyl phenol ethoxylates, alkyl sulfates, and alkyl ethoxy sulfates [84]. The biodegradability of certain surfactants (linear alkyl benzene sulfonates) in environmental matrices, which is dependent on their isomerization process is more rapid under aerobic conditions (with removal rate up to 99%) than anaerobic conditions [84]. Thus, linear alkyl benzene sulfonates have short-term persistence in the environment than alkyl phenol ethoxylates, which are further degraded into by-products such as nonyl and octyl phenols, increasing their environmental persistence and bioaccumulation [84,147]. The effect of benzalkonium chloride exposure is evident in soil microbe resistance to antibiotics [84]. Also, alkyl phenol ethoxylate exposure causes the production of vitellogenin in male fishes at low concentrations [148] just as its by-products, nonyl, and octyl phenols have been associated with certain types of cancer and, low sperm count in men [147].

5.7. Flame retardants

These are lipophilic compounds used in applications such as firefighting equipment manufacture, transportation, construction, electrical/electronic industries, etc. [84]. They are designed to provide lifesaving opportunities in a disaster. For instance, they can extend personnel escape time in an industrial fire incident thus, reducing the number of casualties [84]. Flame retardants enter the wastewater treatment plants through the drainage system and because of their lipophilic (hydrophobic) nature, they are trapped in sewage sludge and reach the environment through biosolid land application, incineration, plastic, and e-waste recycling, etc. [84]. Common flame retardants such as organo-phosphate and brominated flame retardants (BFRs) [84] have long-term persistence in the soil and will undergo transformation, translocation, sorption, and root-uptake processes once in the environment [149]. They negatively affect public health and are toxic to the environment [84].

5.8. Endocrine-disrupting chemicals

These are natural (e.g. daidzein, coumestrol, and genistein found in human and animal foodstuff) or synthetic (e.g. bisphenol, perchlorate, and polychlorinated biphenyls used in manufacturing plastics, epoxy resins, lubricants, industrial solvents, pesticides, electrical equipment, and will certain pharmaceuticals) organic chemicals found in industrial/domestic wastewater, sewage sludge, and biosolids and, can impede the normal functioning of the endocrine or hormonal system [84,150]. These chemicals, which are examples of a group of PoPs found in biosolids, get into the environment via waste discharge including sewage effluent disposal and biosolid land application [151], and are extremely stable and persistent, resulting in high bioaccumulation [84]. The accumulation of endocrine disruptors (EDs) has made them ubiquitous and human exposure pathways included ingesting contaminated food, and water, breathing contaminated air, and contact with domestic/industrial chemicals [84]. Exposure to bisphenol can lead to infertility and the early onset of puberty in adolescents [84] while high levels of perchlorate impede thyroid gland iodine intake, reducing the production of hormones in the thyroid gland [97].

6. Regulations on biosolid land application

For the benefits of biosolid application in agriculture and land reclamation to be fully realized while mitigating its adverse effects on humans and the environment, government agencies around the world have promulgated guidelines for biosolid application practices [152]. Some of these legislations are examined in the following section.

6.1. The sludge directive and regulations (directive 86/278/EEC)

Biosolid land application in the European Union (EU) is controlled by the number of heavy metals it contains which is specified in the EU regulation called The Sludge Directive or simply, The Directive, first enacted in 1986 [153]. This regulation sought to promote sustainable biosolid use in agriculture and control its land application in order to prevent harmful effects on public health and environmental contamination; since treatment and recovery of biosolid on land is one of its important uses [154,155]. Contaminants such as organic compounds and pathogens also present in biosolids, are not considered under The Sludge Directive [18]. Since the enactment of the regulation, the United Kingdom (UK) has made great improvements in the heavy metal content (measured in mg/kg dry solids) of biosolids used for land application as seen in Fig. 10, which showed that between 1982 and ’83, the concentration of Zinc, Copper, Lead, and Chromium allowable in biosolid were 1200, 650, 400, and 130 mg/kg dry solids compared to more recent years between 2001 and 2007, when the allowable concentration of these metals had been scaled down to 650, 300, 150, and 100 mg/kg dry solids respectively, as a way of reducing their environmental impact [50]. The Sludge Directive specified that the soil and biosolid samples are to be analyzed (Table 3) before biosolid usage on land to limit heavy metal concentrations below maximum permissible levels in the soil (Table 4) [156].

Fig. 10.

Heavy metal improvement in biosolid in the UK over a period of two decades [50].

Table 3.

Soil and Biosolid analyses as stipulated by The Sludge Directive [156].

S/N	Soil Analysis	Sludge Analysis
Frequency	Determined by soil mass.	Bi-annually or annually if there's no change in parameters.
Sampling method	Samples should be taken from 25 cm below the surface and not less than 10 cm minimum depth, a minimum of 25 core samples of soil over an area of 5 ha should be taken.	Wet or dry sludge samples can be used for analysis.
Parameters	To be tested should include Zn, Pb, Ni, Cd, Cu, Cr, and pH.	Should include organic matter, pH, dry matter, Zn, Pb, Ni, Cd, Cu, Cr, pH, Hg, N, and P.
Test method (s)	Atomic absorption spectrometry	Atomic absorption spectrometry, Spectrophotometry.

Table 4.

The EU Council standard limit for heavy metals in soil and biosolid for agricultural applications.

Parameter	Soil (mg/kg dm)	Sludge (mg/kg dm)	Loading Amount (kg/ha/yr)
Hg	1–1.5	16–25	0.1
Cd	1–3	20–40	0.15
B	30–75	300–400	3.0
Cu	50–140	1000–1750	12.0
Pb	50–300	750–1200	15.0
Zn	150–300	2500–4000	30.0

The standard permissible limits for heavy metals in soil and biosolid samples used for agricultural applications in 1986, according to The Sludge Directive are given in Table 4; the high concentrations of metals allowable in both soil and sludge samples are noticeable from this table. Although this regulation is almost four decades since it was first enacted, it is still relevant as many other regulations on biosolid reuse have been derived from it (EU member states' individual regulations) [35], its provisions may be reviewed and updated to meet present-day realities [155]. With new and emerging pollutants not covered by the regulation now discovered in biosolids [[86], [87], [88],136,144,145], any potential environmental pollution caused by biosolid samples containing these pollutants will affect far more people in the world today, with the population in 2023 put at 8,045,311,477, at a percentage growth rate of 0.88% than in 1986 (year The Sludge Directive was passed) when the world's population was just 85,804,185 and 2.65% growth rate (Fig. 11) [157].

Fig. 11.

World population data from 1950 and projections up to the year 2100 [157].

[156].

EU member states have scaled down the concentration level of heavy metals in biosolids since the enactment of The Sludge Directive, by promulgating individual national legislations on further reduction in the limits of these metals, keeping values lower than the EU Council's directive, in a bid to further protect humans and the environment (Fig. 12a, b, c, and d showed the comparison of standard limits of selected heavy metals) [35]. In Fig. 12, it can be seen that the majority of EU states including Belgium, Croatia, Denmark, Finland, Germany, Hungary, Latvia, Malta, Netherlands, Slovakia, etc., allowed a national standard limit of heavy metals much below the EU Council's lower limit, which is shown on the figure by the red dotted lines (upper and lower limits). The comparison in Table 5 is important as it gives a glance-view of the national heavy metal standard limits and organic compounds concentration between EU member states.

Fig. 12.

a: Comparison of the limits of (i) Cadmium and (ii) Copper in biosolid for land application set by EU member states and that set by the EU council's Sludge Directive. Red dotted lines represent the EU Sludge Directive's lower and upper limits. b: Comparison of the limits (in mg/kg dw) of (i) Nickel and (ii) Lead in biosolid for land application set by EU member states and that set by the EU council's Sludge Directive. Red dotted lines represent the EU Sludge Directive's lower and upper limits. c: Comparison of the limits (in mg/kg dw) of (i) Mercury and (ii) Chromium in biosolid for land application set by EU member states and that set by the EU council's Sludge Directive. Red dotted lines represent the EU Sludge Directive's lower and upper limits. d: Comparison of the limits (in mg/kg dw) of (i) Zinc and (ii) Arsenic in biosolid for land application set by EU member states and that set by the EU council's Sludge Directive. Red dotted lines represent the EU Sludge Directive's lower and upper limits [35].

Table 5.

Comparison of the standard limits of heavy metals and organic compounds in biosolid among EU states with the EU Council's Sludge Directive.a, b, c, d, etc. represents values from different categories measured. PCDD/F: polychlorinated dibenzo-p-dioxins and furan; AOX: absorbable organic halogens; DEHP: di (2-ethylhexyl) phthalates; NP: nonylphenols; PCB: polychlorinated biphenyls; NPE: nonylphenol ethoxylates; PAH: polycyclic aromatic hydrocarbons; LAS: linear alkylbenzene sulfonates [18].

Permissible heavy metal constituent of biosolid shown in Table 4 (EU Council Sludge Directive, data from 1986), Table 5 (national regulation of EU member states, data from 2019) and Fig. 12 revealed a significant reduction over 3 decades, indicative of the need for lower values and thus, better environmental health. Maria et al. [18] provided the standard limit for pathogens in biosolids in selected EU states based on national legislation, which is not captured by The Sludge Directive. This is represented in Table 6. Data in Table 6 showed that most pathogen standard limits allowable in biosolids are less than or equal to 1000 CFU per gram dry matter (CFU/gDM); this has been adopted in many other states in Europe today [18].

Table 6.

Standard limit for pathogens in Biosolids used in agriculture in the EU.1 = three regions were involved in measurement, 2 = advanced sewage sludge treatment was employed; DM: dry matter; CFU: colony-forming unit; MPCN: most probable cytopathic number u.m.: units of measure; WW: wet weight; MPN: most probable number [18].

6.2. The 40 CFR part 503 regulation

The United States Environmental Protection Agency (USEPA) developed a regulation titled Standards for the Use of Sewage Sludge (popularly referred to as the Part 503 Rule, enacted in 1993), as part of the Clean Water Act of the U.S. Congress [158]. The Rule specifies general minimum requirements for applying biosolids on land for agronomic applications in the United States [159,160]. According to the Part 503 Rule, biosolids used for agricultural applications must meet the ceiling concentration (maximum limit) for heavy metal content before usage; this is given in Table 7.

Table 7.

The EPA Part 503 heavy metal requirements in biosolids applied to land.

Type of Heavy Metal	Concentration limits for all biosolid types applied to land. (mg/kg)a	Concentration limits for exceptional quality (EQ) and pollutant concentration biosolids (mg/kg)a	Cumulative pollutant loading rate (CPLR) limits for biosolid (kg/ha)	Annual pollutant loading rate (APLR) for biosolids (kg/ha.yr)
Chromium	3000	1200	3000	150
Arsenic	75	41	41	2.0
Cadmium	85	39	39	1.9
Mercury	57	17	17	0.85
Lead	840	300	300	15
Copper	4300	1500	1500	75
Nickel	420	420	420	21
Molybdenumb	75	–	–	–
Zinc	7500	2800	2800	140
Selenium	100	36	100	5.0
Applies to:	All biosolids applied on land.	Bulk and bagged biosolids.	Bulk biosolids	Bagged biosolidsc.

ab,c = Dry mass basis measurement; molybdenum limits were deleted from the Part 503 Rule after February 1994 amendment, awaiting EPA consideration; biosolids delivered in bags or other similar containers [159].

The 40 CFR Part 503 Rule specifies pathogens reduction in two biosolid categories, Class A and Class B biosolids. The Rule specifies that pathogens in Class A biosolids be reduced below detectable concentrations [160]. In Class B biosolids, however, pathogens are reduced to concentrations unlikely to pose threats to the environment and public health [160]. There are, however, new pathogens (hepatitis A virus and adenovirus) with heat-resisting capabilities that have been detected in biosolids since the enactment of the Part 503 Rule in 1993 [161]. The general requirements for land application of biosolids based on the Part 503 Rule specified that the supplier of biosolid must provide the user with a guide so as to comply with the requirements of Table 7 and the user, on the other hand, must apply biosolids to meet these requirements [159,162]. The supplier must notify government authorities in writing, about the location and time of application, and provide contact information while the user, must notify authorities before the initial application of bulk biosolids [159].

The majority of literature reviewed for this study agreed that The Sludge Directive (i.e. Directive 86/278/EEC) regulations and the Part 503 Rule formed the basis for biosolid use on land in most countries around the world including developing countries [153,154,[160], [161], [162]]. Iranpour et al. [163], compared the standards (Table 8) specified by both regulations and, a national standard of the Netherlands in a review study in which values for heavy metals were normalized against the U.S. pollution standard limit. These pictorials clearly showed that the national limit of the Netherlands is much lower than EU or U.S limits., further underscoring efforts by EU member states to reduce national pollutant standards for better protection of the environment. Also, Table 8 showed that concentration limits in the EU are expected to reduce significantly, over a long-term period [163].

Table 8.

Comparison of heavy metal standard limits for the EU, Netherlands, and the U.S.

Heavy Metal	EU Limits					Netherland Limits	U.S. EPA Limits
	Upper Limits	Lower Limits	Short-term Limits	Medium-term Limits	Long-term Limits		Ceiling Concentration	Limit Concentration
Chromium	–	–	1000	800	600	75	–	–
Arsenic	–	–	–	–	–	15	75	41
Cadmium	40	20	10	5	2	1.25	83	39
Mercury	25	16	10	5	2	0.75	57	17
Lead	1200	750	750	500	200	100	840	17
Copper	1750	1000	1000	800	600	75	4300	1500
Nickel	400	300	300	200	100	30	420	420
Molybdenum	–	–	–	–	–	–	75	–
Zinc	4000	2500	2500	2000	1500	300	7500	2800
Selenium	–	–	–	–	–	–	100	100

[163].

According to Iranpour et al. [163], the EU Council proposed a reduction in heavy metal concentration in biosolids over a 10-year period in line with member states’ leanings. Iranpour and co-researchers compared these proposed (projected) standards with mean values from the U.S. EPA National Sewage Sludge Survey (NSSS), Pennsylvania, and Los Angeles Surveys over a given period (Table 9). The authors observed a general decline in the value of heavy metals except for Pennsylvania (95th percentile) which has the highest values in spite of the average. They concluded that if the U.S. is to adopt EU proposed limits, new technologies (such as adsorption or precipitation from a suitable porous solid) must be developed to further reduce pollutant concentrations in biosolids.

Table 9.

Comparison of EU projected heavy metal limits in biosolid to U.S. current average values. NSSS = National Sewage Sludge Survey; TITP: Terminal Island Treatment Plant [163].

7. Discussion

In terms of agronomic usage and as a fit for the circular economy, biosolid has had beneficial applications, whether in agricultural land application or as a base material for the manufacture of construction materials. It has been used as organic fertilizer (due to their high organic matter and nutrient content, which is slowly released to plants, making biosolids better than chemical fertilizers in preventing the leaching of nutrients to surface water), as soil amender, and as a land repairer. Although biosolids are treated before land application, they still contain low concentrations of harmful emerging and persistent organic pollutants (PoPs) (Table 2) including per- and poly-fluoroalkyl substances (PFAs), heavy metals, P&PCPs, and microplastics, etc., which can have hazardous effects on humans, animals, and the environment at high concentrations without controlled application of biosolids. Some of the effects in the soil include reproductive defects, neurological development delays, low birth weight, bone variation, accelerated puberty, changes in liver and kidney functions, thyroid disease, and testicular cancer caused by PFAs; algal invasion, endocrine disruption, carcinogenic and toxic compound formation such as chlorinated anilines, dioxins, and chloroform, and, chemical bioaccumulation in snails and earthworms caused by the cosmetic antibacterial chemicals TCS and TCC; nervous system disorders, gastrointestinal and kidney dysfunction, immune system dysfunction, skin lesion, birth defect, vascular damage, and cancer caused by heavy metals; water eutrophication and algae invasion caused by excess soil phosphorus content; Toxic Epidermal Necrolysis (TEN) and Stevens-Johnson syndrome (SJS), reduction in red blood cell production, hemolytic anemia, anaphylaxis, etc. These effects on humans and the environment may be mitigated by biosolid land application practices (Section 4.1) which account for the concentration, fate, and persistence of pollutants in the soil and form part of government regulations.

Government regulations are effective in limiting the number of heavy metals, pathogens, and organic pollutants allowable in biosolids applied on land, imposing restrictions on sites, and fostering good agronomic application practices. The EU's Sludge Directive (Directive 86/278/EEC) and USEPA's Part 503 Rule are the two major legislations on biosolid land application from which many countries around the world and even, EU member states have derived national biosolid legislation. A comparison of both legislations revealed that the EU's Sludge Directive specified stricter regulation, with allowable biosolid pollutant concentration values much lower than USEPA's Part 503 Rule (Table 8). Since the enactment of these major legislations (the Sludge Directive was enacted in 1986 and the Part 503 Rule was passed in 1993), there have been new and emerging contaminants detected in biosolids, making it necessary to review and update these regulations to meet current realities and challenges of today's biosolid land applications.

Updating these government regulations (Directive 86/278/EEC and the Part 503 Rule) should focus on their expansion to accommodate specific legislation on new pathogens, organic pollutants, and emerging contaminants such as microplastics and pharmaceuticals. The updated regulations should review downwards, the standard limits of heavy metals in biosolids (with a focus on USEPA's Part 503 Rule with less stringent allowable standard limits) in line with the national regulation of EU member states, using regulations in the Netherlands as a guide (Table 8). The new heavy metal regulations should take into account soil phosphate interaction with metals which causes metal lability in the soil due to high phosphorus content occasioned by the high agronomic loading rate of biosolid on land. Biosolid land application best practices should form an integral part of government regulatory policies on biosolid use.

8. Conclusion and future perspectives

This review study examined the fate of contaminants in biosolids used for land application and the potential effects of this biosolid management practice on humans and the environment while discussing government policies regulating land application. Although there are other methods (including incineration and energy recovery, landfilling, land reclamation, etc.) employed to dispose of the increasing quantities of biosolids generated from large volumes of wastewater treated daily due to an increasing world population, land application on agricultural farms has been adjudged the most economical and sustainable disposal route aside using biosolid as a base material for the manufacture of construction materials. Land application of biosolids is regulated by the government due to the negative effects of its contaminants and the need to protect the environment. Two major biosolid regulations, the EU's Sludge Directive, and USEPA's Part 503 Rule were identified. These regulations require a review and an update, with a focus on USEPA's Part 503 Rule with less stringent biosolid regulations, to meet the current challenges of biosolid land application. The update should include specific regulations on new and emerging contaminants such as microplastics, pharmaceuticals, pathogens, organic pollutants, and other persistent organic pollutants (PoPs) in biosolid, further reduction of heavy metal standard limits (which should be lower than the projected EU regulation in Table 9), and consideration of soil phosphate-metal interactions to regulate biosolid agronomic loading rate. Future biosolid research should focus on the concentration of TCS, TCC, and newly discovered pharmaceuticals, as well as Microplastic transport in biosolid-amended soils, soil-plant transfer mechanism, and metabolism of PFAs in soils, all of which should inform government policies on biosolid application on land.

Author contribution statement

All authors listed have significantly contributed to the development and the writing of this article.

Data availability statement

Data will be made available on request.

Declaration of competing 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.