The Recovery of Vermicompost Sewage Sludge in Agriculture

Abstract

Considering that worldwide the amount of sludge from sewage treatment plants has increased, which through storage pollutes the environment, solutions must be found for its management. In this paper, through an analysis of studies from the literature, we present an ecological method of recovery of sewage sludge (SS) in agriculture through vermicomposting with Eisenia etida, Eisenia andrei, Eudrilus eugeniae and Perionyx excavatus earthworms, thus we analyzed the possibility that sewage sludge can be transformed from waste into quality fertilizer that benefits the soil, plants, and people, thus being able to replace chemical fertilizers which, if applied to the soil, can acidify and pollute the soil and agricultural crops. We observed that the total nitrogen content of the phosphorus increased. Through the vermicomposting process, organic substances are rapidly decomposed and nitrogen mineralization is accelerated. We studied the impact of dewatered sewage sludge vermicomposting on pH value, electrical conductivity, porosity, moisture content, nitrogen content, water retention capacity, metal content, and the development of agricultural crops, highlighting the positive impact of vermicompost application on the soil. Adding vermicompost to the soil has been observed to improve plant development.

1. Introduction

The increase in the amount of sewage sludge together with the increase in the population in the cities, requires that this sludge be stored, thus putting pressure on the underground and surface waters, but also on the air through the pollutants that drain from this sludge [1].

Wastewater treatment results in two fractions of substance, one liquid (water) and one solid-wet (sludge), known as by-product or waste of the treatment plant [2,3].

The heavy metals contained in the wastewater end up in the sewage sludge, therefore drying, composting, and anaerobic digestion treatments must be applied to them [4].

The correct management of sludge must be done by the following: reduction (by drying), reuse (the biosolid), and recycling (the wet fraction) [2].

Sludges contain the following nutrients beneficial for fertilization: organic matter, fertilizing elements (nitrogen, potassium, phosphorus), and microelements (iron, manganese, copper, molybdenum) [5] necessary for plants [6] that can help increase crop yields and improve soil quality [7,8].

It also contains toxic metals, persistent organic compounds, pathogenic bacteria, and parasite eggs, which can pollute the soil and groundwater [9].

Vermicomposting of sewage sludge with the earthworm Eisenia fetida is an ecological method of sludge management; the worms break down the organic matter, modify it biologically, physically and chemically, the C:N ratio is reduced, the content of N and P is increased, the pathogenic load of various wastes, obtaining a quality fertilizer for the soil [10]. Pathogenic agents, salmonellae bacteria, viruses, and parasitic worms Ascaris spp are reduced, and the unpleasant smell is eliminated.

Earthworms transform, ingest, grind, and digest organic waste with the help of micro-flora in the intestine, turning it into a fine, moistened vermicompost. Pathogens (bacteria, viruses, fungi, and parasites) may be present in certain organic wastes. These pathogens when entering the soil, water, or air can have a negative impact on health [11].

According to the research by Adhikary [12], in the process of vermicomposting, pathogens enter the trophic chain of earthworms, achieving rapid sanitation of waste, and the volume of waste is reduced by 40–60% [12]. Earthworms feed on cattle manure, pig manure, fungi, protozoa, fresh food waste, and sludge from the paper and tannery industries [13]. Vermicomposting must be carried out in spaces protected from rain and sun [14,15,16]. The most used earthworm for vermicomposting is Eisenia fetida [13].

One ton of vermicompost (biohumus) contains 35–40 kg of NPK, (nitrogen, phosphorus, potassium), a quality organic fertilizer. Recommended amounts of vermicompost are: 2–3 tonnes/ha (0.2–0.3 kg/m²) for fertilizing annual crops, 0.5–1.5 kg for each tree and vine and 3.5–5.0 tons/ha when fertilizing soil in greenhouses [17].

The application of chemical fertilizers on the soil, over time, leads to soil acidification, carbon loss, soil erosion, and the loading of agricultural crops with pollutants.

Since the production of sludge from wastewater treatment plants is high, the uncontrolled storage of sludge can affect the underground water and the surface water, and it can pollute the air. In this work, we analyze the management of SS by vermicomposting with the earthworm Eisenia fetida, thus eliminating the problem of sewage sludge storage and environmental pollution, obtaining a quality fertilizer for the soil.

Through this sewage sludge treatment technology, unwanted odors, pathogens, and high concentrations of heavy metals are eliminated [18,19].

2. Eisenia fetida

The earthworm Eisenia fetida (Figure 1) lives in soil and in manure, has a length of 26–150 mm and a diameter of 2–6 mm, can live for 28 months, and the use of this earthworm in vermicomposting causes an increase in carbon content and total nitrogen [17,20,21].

The vermicomposting process is carried out at temperatures higher than 15 °C [3], because at low temperatures the development of earthworms stops [17].

The efficiency of the vermicomposting process decreases with decreasing temperature, so the recommended temperature is between 12 °C and 28 °C. Eisenia fetida can live at temperatures between 0–35 °C, and it can die at temperatures higher than 35 °C [3,5,17].

The pH of the worm bed should be maintained at 6.8–8. The pH of the vermicompost should be measured weekly [3], the pH of the worm bed decreases over time. At a salinity of 0.2%, the worms had the highest weight, while at a salinity higher than 0.2%, the cells of the worms can be dehydrated due to the imbalance of the osmotic pressure [22]. To reduce the salt content below 0.2% [22] and to maintain adequate humidity (60–80%), the litter on which the earthworms sit must be watered [22]. The total mortality of the worms was found at a soil salinity gradient with an electrical conductivity of 1.31 dSm⁻¹, their survival being affected at values of 0.92 dSm⁻¹.

The growth of E. fetida was affected at electrical conductivity values lower than 1.03 dSm⁻¹ [23]. According to [24], at soil salt concentrations of 1 and 15 g/kg, worm survival was 90%.

The mass of earthworms is 0.5–0.6 g [14].

Earthworms Eisenia fetida reproduce very quickly if they have good conditions. Earthworms die at high or very low temperatures in the absence of moisture and oxygen, as they breathe through the skin.

During the vermicomposting process, earthworms double every 60–90 days, so that reproduction does not stop [16,17,25,26]. It is recommended that the initial density of earthworms does not exceed 4 kg/m² [3]. They must have enough space; the amount of worms recommended in the case of vermicomposting is 2.0–4.0 kg m⁻², and for vermiculture 0.5–2.0 kg m⁻² [27]. A high stocking density [17,18,19,20,21,22], vermicomposts produce a small amount of waste [25,26,27,28,29,30], and a lower removal of pathogens [31,32].

The content of ammoniacal nitrogen in the sewage sludge must be less than 200 ppm; it increases with the increase in the temperature of the vermicompost and the pH value [33]. At the completion of vermicomposting, the amount of worms is reduced and they can die at high pH values of 8.3–9.5 and at high $N{H}_4^{+}$ concentrations due to the mineralization of waste proteins [34].

During vermicomposting, earthworms feed on toxic organic waste, biochemically degrade sewage sludge [13,34], homogenize the material through the muscular actions of the intestine, and release nutritious vermicompost for soil and plants [3]. E. fetida worms increase in weight by 5 and 20 g [35,36].

Figure 1 describes the processes through which the vermicomposting of waste is carried out by the earthworm E. fetida [37]. The worm Eisenia fetida bioaccumulates metals through the skin and through digestion [38,39].

Figure 1. The process of vermicomposting by earthworms (adapted from [36]).

Figure 1. The process of vermicomposting by earthworms (adapted from [36]).

3. The Physico-Chemical Properties of the Vermicompost SS

In this work, the sludge from urban wastewater treatment plants that have a water content of 70–90% is analyzed [37,38,39,40]. The composting process lasted 56 days [41] and 90 days [42]. The pH of the sewage sludge was between 6.77–7.68, and that of the vermicompost was 5.24–8 [41]. Before vermicomposting, precomposting was carried out for 14 days to annihilate pathogenic bacteria and to decrease the content of NH₃ which is dangerous for earthworms. Vermicomposting was carried out at a temperature of 23 °C and a relative humidity of 70–80% [43].

Table 1. Physico-chemical characteristics of simple and vermicomposted SS (data from [10,34,41,42,43,44,45]).

Description	Humidity (%)	EC (μs/cm)	OM (%)	pH	TOC (%)	N (%)	C/N	P (%)	Ash (%)	R
VDS Ef	NM	3990 ± 47	NM	5.49 ± 0.01	253.2 ± 3.8	35.58 ± 0.7	7.11	NM	NM	[10]
SSS	NM	1071 ± 21	NM	6.77 ± 0.01	368.5 ± 2.0	35.80 ± 0.3	10.29	NM	NM	[10]
VDS Ef	70	NM	NM	7.0 ± 0.04	220.8 ± 1.6	28.8 ± 2.7	7.7 ± 0.3	46.7 ± 0.24	NM	[42]
SS	65	NM	NM	7.2 ± 0.03	242.0 ± 2.81	27.4 ± 0.29	8.8 ± 0.13	44.2 ± 0.1	NM	[42]
VDS Ef	32.2 ± 3.4	358 ± 4	67.8 ± 3.2	8 ± 0.5	37.6 ± 2.2	2.6 ± 0.5	14.5 ± 2	0.5 ± 0.3	32.2 ± 1.5	[41]
SSS	48.2 ± 1.4	1041 ± 15	90 ± 1.2	7.3 ± 0.5	50.3 ± 0.8	2.2 ± 0.4	22.5 ± 3	0.3 ± 0.2	9.4 ± 1.6	[41]
VDS Ef	21.2 ± 3	636 ± 12	63 ± 3	7.7 ± 1.2	33.5 ± 2.5	2.2 ± 0.3	15 ± 6	0.6 ± 0.2	39.5 ± 1.8	[41]
SSS	53.8 ± 5	1485 ± 6	80.5 ± 3	6.7 ± 0.8	44.5 ± 1	1.5 ± 0.1	26.5 ± 8	0.4 ± 0.1	19.5 ± 1.5	[41]
VDS Ef	81.4 ± 0.4	NM	54.1 ± 0.5	5.24	26.3	2.7	9.7	29.5 ± 0.7	45.9 ± 0.5	[43]
SSS	78.9 ± 0.3	NM	63.6 ± 0.7	7.68	35.3	4.6	7.7	23.5 ± 0.7	36.4 ± 0.7	[43]
SSS	NM	NM	NM	6.30 ± 0.27	285.8 ± 11.44	15.68 ± 0.48	18.25 ± 1.31	5.60 ± 2.00	NM	[44]
VDS Ef	NM	NM	NM	5.66 ± 0.02	276.88 ± 6.13	15.96 ± 0.00	17.35 ± 0.38	4.76 ± 0.11	NM	[44]
VDS Ea	NM	NM	NM	5.64 ± 0.02	272.56 ± 7.46	9.94 ± 1.11	27.59 ± 2.22	4.06 ± 0.04	NM	[44]
SSS	NM	2800 ± 0.08	NM	6.88 ± 0.1	33.54 ± 0.44	1.31 ± 0.1	25.6 ± 1.5	7.97 ± 0.1	42.16 ± 0.5	[34]
VDS Ef	NM	5000 ± 0.11	NM	6.7 ± 0.1	30.1 ± 0.2	3.2 ± 0.23	9.8	14.6 ± 0.2	47.9 ± 0.5	[34]
VDS Eu	NM	5000 ± 0.09	NM	6.8 ± 0.1	28.2 ± 0.13	3.7 ± 0.24	7.8	12.6 ± 0.2	51.3 ± 0.7	[34]
VDS P.ex	NM	5000 ± 0.12	NM	6.9 ± 0.2	25 ± 0.15	3.6 ± 0.25	7	11.9 ± 0.1	56.8 ± 0.6	[34]
VDS	20–40	≤4000	20–50	5.5–8.54	-	1–4	≤20	-	-	[45]

SSS—sewage sludge samples, VDS Ef—vermicomposted dehydrated sludge with Eisenia fetida, VDS Ea vermicomposted dehydrated sludge with Eisenia andrei, VDS Eu—vermicomposted dehydrated sludge with Eudrilus eugeniae, VDS P.ex—vermicomposted dehydrated sludge with vermicomposted dehydrated sludge with Perionyx excavatus, OM—organic matter, NM—Not Measured, EC—electrical conductivity, R—references.

shows the physico-chemical properties of the sample of simple sludge and vermicompost.

We analyzed the vermicomposting of sewage sludge with Eisenia andrei and Eisenia fetida worms and found according to [44], that in the case of vermicomposting with Eisenia andrei the following values were lower: pH, phosphorus content, nitrogen content, total content of organic carbon, the C:N ratio was lower in the case of vermicomposting with E. fetida. According to [34], during vermicomposting with all types of worms (Table 1), the electrical conductivity of the sludge increased, the ash content increased due to the decomposition of waste and the nitrogen content increased due to the activity of the worms, the phosphorus content increased somewhat more in in the case of E. fetida, the total organic carbon content decreased due to the use of carbon dioxide by the worms, and decreased a little more in the case of vermicomposting with E. fetida and the carbon nitrogen ratio decreased in the case of vermicomposting of the sludge by the three worms. The ash concentration is higher in the vermicomposted sludge compared to the simple sample, due to the decomposition of organic waste by earthworms (Table 1).

According to the values in

Table 2. Soil nutrients (data from [34,41,42,43]).

Description	K (%)	Ca (%)	Mg (%)	P (%)	R
VDS Ef	6.8 ± 0.04	58.9 ± 0.21	13.8 ± 0.1	12.9 ± 0.04	[41]
SSS	6.4 ± 0.04 e	58.7 ± 1.1	12.9 ± 0.1	11.7 ± 0.2	[41]
VDS Ef	3.57 ± 0.20	52.00 ± 2.83	6.1 ± 0.1	29.5 ± 0.7	[43]
SSS	2.70 ± 0.14	47.00 ± 0.00	5.0 ± 0.1	23.5 ± 0.7	[43]
VDS Ef	4.9 ± 0.05	47.6 ± 0.5	24.5 ± 0.5	46.7 ± 0.24	[42]
SSS	5.1 ± 0.05	46.7 ± 0.24	23.7 ± 0.16	44.2 ± 0.1	[42]
SSS	0.86 ± 0.56	5.39 ± 0.68	NM	7.97 ± 0.1	[34]
VDS Ef	1.2 ± 0.87	10.7 ± 0.89	NM	14.6 ± 0.2	[34]
VDS Eu	1.2 ± 0.86	10.3 ± 0.98	NM	12.6 ± 0.2	[34]
VDS P.ex	1.2 ± 0.89	14.5 ± 1.07	NM	11.9 ± 0.1	[34]

R—Reference, SSS—sewage sludge samples, VDS Ef—vermicomposted dehydrated sludge with Eisenia fetida, VDS Eu—vermicomposted dehydrated sludge with Eudrilus eugeniae, VDS P.ex—vermicomposted dehydrated sludge with vermicomposted dehydrated sludge with Perionyx excavatus, NM—Not Measured.

, the concentrations of phosphorus, calcium, magnesium, and potassium in the vermicomposted sludge sample were higher than those in the sewage sludge sample, due to the action of the bacteria during vermicomposting [43,46].

Calcium content increased slightly during vermicomposting of sewage sludge due to the action of earthworms that converted part of the calcium from bound to free form [47].

By adding an amount of vermicompost to the soil, tomato seeds germinated faster than in the simple soil sample [48,49]. It was found that adding vermicompost to the soil improved the physical and chemical properties of the soil [4].

According to [34,41,42,43], after vermicomposting the sludge with Eudrilus eugeniae worms, with Perionyx excavatus, and with E. fetida, the nutrient content increased (Table 2), and the higher phosphorus values were obtained in the case of using E. fetida.

3.1. The Impact of Vermicomposting on the pH of SS

According to studies carried out by [41,43], at the end of vermicomposting due to the production of CO₂ [35], the pH values of the sewage sludge increased compared to those of the soil sample [41,43].

The reduced pH values during vermicomposting may also be due to the faster degradation of organic waste by the action of earthworms, compared to the sewage sludge sample without vermicompost [48,50]. With a larger amount of vermicompost added to the soil, a reduction in the pH value was obtained [51]. Through the decomposition of waste, humic acids and ammonium are formed, which change the pH values, making it favorable for the development of plants [49].

Soil pH values influence earthworm reproduction [52,53], high values favor the entry of nanotoxin particles into earthworms, reducing their reproduction rate [54] and metal absorption [55]. Increasing pH value was associated with increasing zinc removal rate from sewage sludge [55]. The decrease of soil pH below 5.8 favors the accumulation of zinc, below 6.3 of nickel, and below 4.5 of copper in the sewage sludge. The transport of metals by sludge in the soil is influenced by the pH values, which should be 6.5 in the case of cultivated soils and 6.0 for grassy lands, for grazing [37]. Lowering the pH reduces the negative effect of metals on earthworms, due to the solubility of toxins [56,57].

3.2. The Impact of the Vermicomposting Process on the Electrical Conductivity of Sewage Sludge

The electrical conductivity values of sewage sludge decreased due to the decomposition of organic matter and the mineralization of compounds by earthworms [34,41].

3.3. The Impact of the Vermicomposting Process on Total Organic Carbon

Total organic carbon concentration in sewage sludge decreased due to decomposition and mineralization of organic matter by earthworms, worms, and microorganisms consume carbon as an energy source [33]. The nitrogen level increased and the C/N ratio decreases during vermicomposting [41].

3.4. Carbon to Nitrogen Ratio (C/N)

The authors [52] reported that this ratio shows the maturity of the vermicompost; maturity is good when the values are less than 20, because for the use of vermicompost in agriculture, the values of the C/N ratio must be less than 15. The values of this ratio, which represent the decomposition of the organic compound, decreased during the process of vermicomposting [52].

3.5. Nitrogen Concentration

In the vermicomposted sludge compared to the control sample, the concentration of nitrogen increased. Nitrogen is necessary for plants to grow. It is observed that the concentration of nitrogen in the vermicomposted sludge sample is higher compared to the control sample; this may be due to the mortality of the worms after 90 days of vermicomposting [42].

3.6. Phosphorus Concentration

Phosphorus concentration decreased due to the adsorption of inorganic phosphorus released from earthworm tissues; there were situations where it increased due to microorganisms and enzymes from earthworms’ intestines [41].

4. The Content of Heavy Metals in Vermicomposted Sludge

SS from treatment plants due to its heavy metal content can have a negative impact on soil and plant development [57].

Earthworms together with microorganisms ingest toxic heavy metals, through feeding and through the skin, through absorption [35].

Zinc can regulate respiration and increase earthworm tissues [35].

The reduction in the content of metal ions due to the degradation by vermicomposting of organic waste is calculated with Equation (1):

$$Metalcontent=\frac{100}{\left[100-\left(OMini\times \left(\frac{OM\mathrm{deg}}{100}\right)\right)\right]}\times 100$$

(1)

where

OMini—organic materials before vermicomposting (dry weight); OMdeg—decomposition of organic materials after vermicomposting [35].

Vermicasts have organic substances, phytohormones, cytokinins and auxins, which can trigger plant growth [3].

Metals are bioaccumulated in the body of worms through absorption, excretion, storage, and internal distribution.

The absorption rate of metals can be highlighted as follows: [uptake] = [absorption] − [elimination] − [biotransformation] [34].

The bioaccumulation factor (BAF) of heavy metals in earthworms is calculated with Equation (2) [34]:

$$BAF=\frac{C_w(ss)}{C_x},$$

(2)

where: C_w(ss) is the metal concentration contained in the earthworms and C_x is the total metal concentration in sludge (mg metal kg⁻¹ sludge).

The accumulation of heavy metals in 90 days of vermicomposting [36] by earthworms Eisenia fetida is due to their enzymatic activity; neutral pH values favor the accumulation of heavy metals by earthworms [4]. According to the research [39], metals are adsorbed by the worm Eisenia fetida in the following order: Zn > Cu > Pb > Hg.

pH affects cadmium uptake and transformation; pH values in the sludge sample without earthworms added were below 6.5, increasing to 6.7–7.7 when earthworms were added [41,47,58,59,60,61,62,63].

According to the data presented in

Table 3. Values of metal content in the vermicomposted sludge and in the initial substrate (unit: mg/kg dry matter) (data from [34,35,41,44,58]).

Type	Cd	Fe	Cu	Cr	Ni	Pb	Zn	R
VDS Ef	0.68 ± 0.051	NM	37 ± 4.69	NM	10.04 ± 0.51	45 ± 2.73	109.85 ± 7.18	[35]
SSS	2.57 ± 0.07	NM	105 ± 10.92	NM	68.73 ± 7.83	116 ± 8.47	265 ± 19.22	[35]
VDS Ef	0.8 ± 0.5	4412 ± 15	NM	0	0	2 ± 0.3	NM	[41]
SSS	1.7 ± 0.4	6098 ± 35	NM	27 ± 2	16.8 ± 7	16 ± 7	NM	[41]
VDS Ef	0.12 ± 0.1	1506 ± 6	NM	0	0	0	NM	[41]
SSS	0.6 ± 0.2	3927 ± 8	NM	9.5 ± 0.4	19.8 ± 1.2	13.4 ± 3	NM	[41]
S pH > 6.5	20	NM	500	NM	200	1000	1000	[35]
S pH < 6.5	5	NM	250	NM	100	300	500	[35]
S	1–3	NM	50–140	-	30–75	50–300	150–300	[58]
SSA	20–40	-	1000–1750	-	300–400	750–1200	2500–4000	[58]
SSS	1.05 ± 0.11	NM	120.69 ± 15.49	NM	10.53 ± 0.38	44.33 ± 4.75	509.72 ± 92.12	[44]
VDS Ef	0.89 ± 0.01	NM	115.18 ± 0.81	NM	10.35 ± 1.17	43.27 ± 0.53	550.78 ± 4.48	[44]
VDS Ea	0.99 ± 0.03	NM	99.1 ± 0.50	NM	8.13 ± 0.13	36.6 ± 1.94	465.72 ± 5.14	[44]
SSS	NM	0.63 ± 0.03	158.2 ± 20	NM	NM	49.4 ± 6	612 ± 45	[34]
VDS Ef	NM	0.97 ± 0.06	158.2 ± 27	NM	NM	30.6 ± 3.8	513 ± 42	[34]
VDS Eu	NM	0.98 ± 0.06	157.2 ± 25	NM	NM	36.6 ± 3.2	498.26 ± 35	[34]
VDS P.ex	NM	0.95 ± 0.05	136.4 ± 31	NM	NM	35.8 ± 2.5	473.2 ± 31	[34]

R—references, S—soil, SS—sewage sludge, SSA—sludge for for use in agriculture, VDS Ef—vermicomposted dehydrated sludge with E. fetida, VDSEa—vermicomposted dehydrated sludge with Eandrei, VDS Eu—vermicomposted dehydrated sludge with Eudrilus eugeniae, VDS Eu—vermicomposted dehydrated sludge with Eudrilus eugeniae, VDS Pex—vermicomposted dehydrated sludge with vermicomposted dehydrated sludge with Perionyx excavatus, NM Not Measured, SS—Simple soil.

, the concentrations of metals in the vermicomposted sludge are lower compared to those in the sludge sample [29,53,58,59].

We analyzed the vermicomposting of sewage sludge with Eisenia andrei and Eisenia fetida worms and found that, according to [44], the concentration of metals in the sewage sludge decreased in both cases and cadmium decreased slightly more in the case of vermicomposting with E. fetida (Table 3). The bioaccumulation of metals in the body of E. fetida and E. andrei worms was thus Cd > Zn > Cu > Ni > Pb. And in vermicomposting with worms Eisenia fetida and Eudrilus eugenia [64], both accumulated metals from sewage sludge. The values of the concentrations of heavy metals in the sewage sludge presented in this work were lower than those provided in the standard [59].

According to [34], the concentration of metals decreased when vermicomposting with all worms with Eudrilus eugeniae, with Perionyx excavatus, and with E. fetida slightly more in the case of lead (Table 3).

According to 64, by vermicomposting with Eudrilus eugeniae, the Cd content in the sludge decreased from 1.31 ± 0.13 mg/kg to 0.20 ± 0.02 mg/kg, chromium decreased from 41.24 ± 3.90 mg/kg to 4.44 ± 0.50, lead decreased from from 31.22 ± 3.20 mg/kg to 10.17 ± 1.1 mg/kg and zinc decreased from 347.20 ± 32.5 to 124.40 ± 11.31 mg/kg. Through vermicomposting with E. fetida, the cadmium content decreased from 1.26 ± 0.11 mg/kg to 0.11 ± 0.01 mg/kg, chromium decreased from 40.99 ± 3.90 mg/kg to 6.34 ± 0.42 mg/kg, lead decreased from to 31.21 ± 2.9 mg/kg to 8.11 ± 0.75 mg/kg and zinc decreased from 356.34 ± 32.51 mg/kg to 111.97 ± 10.32 mg/kg.

We analyzed the vermicomposting of sewage sludge with Eisenia fetida and Eudrilus eugeniae worms and found that according to [64], According to 64, the concentration of chromium in the body of the worm E. fetida was 0.54 ± 0.03, of lead was 0.98 ± 0.08 mg/kg, of zinc was 106.4 ± 10.5, and in the body of the worm Eudrilus the concentration of chromium was 0.52 ± 0.04 mg/kg, lead 0.75 ± 0.05 mg/kg and zinc was 98.23 ± 8.5 mg/kg. Higher concentrations of metals, according to 64, were adsorbed by E. fetida. E. fetida accumulated more metals compared to Eudrilus eugeniae, and the bioaccumulation factor was higher in the case of E. fetida.

Zinc was the only metal that exceeded the standard limit value [58].

Vermicompost contains phosphorus, nitrogen, and other nutrients for the soil; earthworms bioaccumulate the metals, thus being able to replace chemical fertilizers [59] (

Table 4. The values of the metal content accumulated by Eisenia fetida at the end of the vermicomposting process (unit: mg/kg, dry weight) (data from [35]).

Type	Cr	Cd	Cu	Ni	Pb	Zn	R
Ef	NM	7.64 ± 0.35	89.93 ± 7.82	39.54 ± 1.78	51.33 ± 1.97	348.75 ± 23.86	[35]
BAF Ef	NM	2.973	0.856	0.575	0.443	1.316	[35]

SSS—sewage sludge samples, V—vermicompost sludges, Ef—Earthworm E. fetida body tissues (mg/kg), BAF Ef—The bioaccumulation factor for Eisenia Fetida, NM—Not Measured.

) [34]. The amount of metals absorbed by earthworms depends on the organic carbon content and the pH of the sludge [42].

It was observed that the earthworms accumulated heavy metals; at the end of the vermicomposting process was a high content of cadmium and zinc followed by copper and nickel (Table 4) [62,63,64,65].

The land application of sewage sludge without being vermicomposted would pollute soil and agricultural crops due to metal content [66].

At the end of vermicomposting, bioaccumulation had values between 0.443 and 2.973, and high metal concentrations in soil lead to low BAF [35]. BAF can have values lower than 0.1, and higher than 10, depending on the amount of metals and the type of worms [35]. To remove excess bioaccumulated metals [67] as in the case of copper and zinc, an initial rapid uptake by earthworms was followed by an equilibrium period. For cadmium bioaccumulation, excretion was slow or absent [68]. For Zn, although concentrations are high, BAFs were lower in polluted soils. Excreting some of the zinc could help regulate metal concentrations in earthworms. Eisenia fetida can accumulate some nickel [34].

In the vermicomposting process, earthworms transform sewage sludge into high-quality fertilizer for soil and agricultural crops [65]. The number of worms decreases during vermicomposting if only sewage sludge is used without any other waste mixture, if the worms do not have enough food [65].

In 90 days of vermicomposting the sewage sludge, the biomass of worms increased by 101.0 ± 7.3 mg, starting from a mass of 292.5 ± 1.7 mg; the growth rate of each worm was 1.13 ± 0.07 mg day⁻¹, 55.0 ± 13.2% worms died during vermicomposting and the reproduction rate of worms was 0.017 ± 0.009 cocoons worm⁻¹ day⁻¹) [42].

Zhao et al. [62] observed that the earthworms transformed the insoluble organic matter into soluble so that it could be degraded increasing the microbial activity. They stimulated the development of the good bacteria Pro-teobacteria and Pseudomonas sp. The earthworms digested the sludge with sizes between 10–200 mm, transforming the sludge into fine sizes of 0–2 mm and the microorganisms fed on this fine sludge which could be further decomposed by microbes [62].

5. The Impact of Using Vermicompost Sewage Sludge on Plant Growth

Vermicompost, due to its nutrient content, stimulates the development of the following crops: tomatoes [67], pepper [68], garlic [69], sweet corn [70], eggplant [71], bananas [72], Chinese cabbage [73], spinach [74], and lettuce. It stimulates the development of chrysanthemum, marigold, geranium, petunia, and poinsettia flowers, and stimulates the development of acacia, eucalyptus, and pine trees [67].

Vermicompost has a positive impact on plants (leaf surface, root volume, root branching) due to the macro and micronutrients it contains, it improves the biological functions of the soil.

The application of vermicomposted sludge to the soil improved the growth of barley and cereal plants compared to those that grew in the plain soil sample [9].

After applying an amount of vermicompost, similar to 200 kg ha⁻¹ of nitrogen, on an agricultural soil cultivated with corn, improvements in soil porosity were found [67]. The use of vermicompost as a fertilizer can have the following advantages: it eliminates harmful insects, it reduces the infestation of plants with diseases due to pathogens, it fertilizes the soil, and it improves the structure of the soil by being a soil amendment [67].

6. Conclusions

From the analysis of the studies presented in this review, regarding the effects of the actions of worms Eisenia fetida, Eisenia andrei, Eudrilus eugeniae, Perionyx excavatus on the sewage sludge can be seen as follows: they biopurify the sewage sludge by accumulating heavy metals through the skin, through food, and through absorption [49]. The sludge was cleaned of pathogenic bacteria, transforming the sludge into a quality fertilizer, rich in nutrients that benefits the soil and crops [75]. In the case of vermicomposting with Eisenia fetida, the parasite eggs were removed after 21 days, and after 120 days pathogens have been reduced [76,77]. Through vermicomposting, the volume of waste is reduced, and there is no need to store the sludge, thus avoiding soil and water pollution [78,79,80].

The bioaccumulation of metals in the body of E. fetida and E. andrei worms was thus Cd > Zn > Cu > Ni > Pb [44]. According to [64], E. fetida accumulated more metals compared to Eudrilus Eugeniae, and the bioaccumulation factor was higher in the case of E. fetida.

Vermicomposting of sewage sludge with E. fetida is a sustainable, economical, and practical method of sewage sludge management [81,82] E. fetida is a worm very often used in vermicomposting [82,83]. The following advantages were obtained in the vermicomposting treatment compared to thermal composting: the weight of the vermicompost is smaller than that of the compost, the processing time is shorter, the nitrogen content is higher, the humus content is higher, the phytotoxicity is lower, fertilization is higher [84] and the growth hormone (kinetin) content of plants is higher [80,81].

The vermicomposts produced meet the limits of the European Union (EU) compost quality standards, being suitable for agricultural use [58]. Before sludge from wastewater treatment plants is applied to agricultural soils, it is important to know the concentration of metals in the sludge to avoid risks to the soil and crops.

Based on what is presented in this review, we believe that by using this ecological method of recovery of the sewage sludge, we protect the environment, we obtain pollutant-free agricultural crops, and ensure proper sewage sludge management. The discussed problem, in connection with the need to minimize the amount of sewage sludge, is constantly being researched by scientists from different regions of the world. A review article on this topic will hopefully be helpful to other researchers interested in this topic.