Component analysis and risk assessment of biogas slurry from biogas plants

Lanting Ke,Xiaobin Liu,Bingqing Du,Yuanpeng Wang,Yanmei Zheng,*,Qingbiao Li,2,*

1 Department of Chemical and Biochemical Engineering,College of Chemistry and Chemical Engineering,Xiamen University,Xiamen 361005,China

2 College of Food and Biology Engineering,Jimei University,Xiamen 361021,China

Keywords:Biogas slurry Antibiotics Heavy metals Risk assessment

ABSTRACT Massive amounts of biogas slurry are produced due to the development of biogas plants.The pollution features and the risk of biogas slurry were fully evaluated in this work.Thirty-one biogas slurry samples were collected from sixteen different cities and five different raw materials biogas plants(e.g.cattle manure,swine manure,straw-manure mixture,kitchen waste and chicken manure).The chemical oxygen demand(COD),ammonia nitrogen (NH+4 -N),anions (e.g.Cl-,SO2-4,NO-3 and PO3-4),antibiotics (e.g.sulphonamides,quinolones,β2-receptor agonists,macrolides,tetracyclines and crystal violet) and heavy metals(e.g.Cu,Cd,As,Cr,Hg,Zn and Pb)contents from these biogas slurry samples were systematically investigated.On this basis,risk assessment of biogas slurry was also performed.The concentrations of COD,NH+4-N and PO3-4 in biogas slurry samples with chicken manure as raw material were significantly higher than those of other raw materials.Therefore,the biogas slurry from chicken manure raw material demonstrated the most serious eutrophication threat.The antibiotic contents in biogas slurry samples from swine manure were the highest among five raw materials,mostly sulphonamides,quinolones and tetracyclines.Biogas slurry revealed particularly serious arsenic contamination and moderate potential ecological risk.The quadratic polynomial stepwise regression model can quantitatively describe the correlation among NH+4 -N,PO3-4 and heavy metals concentration of biogas slurry.This work demonstrated a universal potential threat from biogas slurry that can provide supporting data and theoretical basis for harmless treatment and reuse of biogas slurry.

1.Introduction

Biogas engineering is an environmentally friendly technology.Organic wastes were utilized as digester raw materials of biogas engineering,such as animal manure,seedcase,straw,etc.[1–4].In China,the number of biogas plants has doubled from 2013 to 2020,and the annual production of methane from biogas plants has reached 44 billion cubic meters [5].Meanwhile,biogas plants also generate hosts of biogas slurry and biogas residues,most of which are biogas slurry.Wuet al.[6] found that only 1.7% (mass)methane was obtained,and the proportion of biogas slurry was as high as 87.3%(mass)in the biogas plant.On the basis of the relationship between methane and biogas slurry,the annual output of biogas slurry has exceeded 1.6 billion tons.However,the biogas slurry produced from biogas engineering can contribute to environmental pollution,and improper disposal can lead to a waste of resources [7].Therefore,harmless biogas slurry is important during the rapid development process of biogas plants.

Understanding the composition of biogas slurry is the first step to conduct its harmless treatment.Biogas slurry contains abundant C [8],N [8–11] and P [8,12,13] contents,which are commonly reused as organic fertilizer,as reported in the literatures[10,11,13–19].However,biogas slurry also contains substantial amounts of heavy metals [20–23],such as As,Fe [24,25],Hg,Zn,and Cu [26].The crops watered continuously with biogas slurry may lead to heavy metals accumulation in soil and crops [27–29],which would transfer into the food chain and have potential risk to human beings [22].Plenty of studies have indicated that heavy metals of biogas slurry can be transferred to soil and crops,nevertheless,studies have been rarely conducted on the quantitative evaluation of heavy metal risk in biogas slurry [30].

Antibiotics have been universally used as feed additives in livestock and poultry farming for nearly 30 years [31,32].Similar to heavy metals,antibiotics would also accumulate in the food chain[33].Pinheiroet al.[34] discovered that the antibiotics were detectable in the crops using liquid waste from piggeries as agricultural fertilizer.Although antibiotics have been used in animal feeding since the early 1990s,few reports on the presence of antibiotics residues in agricultural wastewater or slurry are available [35].Information on the antibiotics contents of the biogas slurry from different districts and different raw materials biogas plants is lacking.

In this study,to provide the basic data for the reuse of nutritional ingredients in the biogas slurry,COD,NH+4-N,anions,antibiotics and heavy metals contents of the biogas slurry collected from five different raw materials in sixteen different cities in China were investigated.The features and the risk of biogas slurry were also evaluated.It is very important to clarify the components and quantify the risk of biogas slurry in biogas plants,which will not only expand the cognition of biogas slurry pollution but also provide supporting data and theoretical basis for harmless treatment and reuse of biogas slurry.

2.Experimental

2.1.Sample description and retention

The biogas slurry samples were collected from thirty-one biogas plants in sixteen cities in China.The sample information is shown in Table 1.In addition,sampling address and date are shown in Table S1.Among these biogas plants,seven used cattle manure(CAM) as digester raw material,thirteen used swine manure(SM),four used straw-manure (St+M),three used kitchen waste(KW) and four used chicken manure (CHM).Fresh biogas slurry were obtained from the drainage pipeline of biogas fermentation tank and stored in cooler box (0 °C) straight away.Then the samples were transferred and kept in the refrigerator (-20 °C) with the least delay possible.The slurry samples were analysed within one month [35].The fermentation systems of investigated plants were operated between 25 °C and 55 °C.The pH of slurry was detected by a pH meter (PHS-2F,SPSIC-INESA,China).

Table 1 Sample information of biogas plants

2.2.Sample preparation

The lab wares were dipped in 10%HNO3for more than one day and then washed with deionized water at least five times to be used for biogas slurry samples collecting,storing,handling and analysing.

All biogas slurry samples were centrifuged for 10 min at 10,000 r?min-1.Then,the supernatants were stored in 20 ml serum bottles and kept in the refrigerator (-20 °C).The supernatant was appropriately diluted before the detection.The biogas slurry samples were filtered through 0.22 μm membranes prior to heavy metals,anions and antibiotics analyses.

2.3.Analytical methods

The anions,including Cl-,andwere determined by ion chromatography (DIONEX IC-900,USA).

Liquid chromatography–tandem mass spectrometry (Agilent 6490 Triple Quad LC–MS/MS,USA) was applied to detection of the twelve antibiotics,pigmentum and hormone classes (sulphonamides,quinolones,β2-receptor agonists,macrolides,tetracyclines,β-lactams,crystal violet,male hormone,nitrofuranmetabolites,oestrogen hormone,chloramphenicol and quinoxalines).

Inductively coupled plasma–tandem mass spectrometry(Agilent-7700×,USA) was chosen to assay seven kinds of heavy metals (e.g.Cu,Cd,As,Cr,Hg,Zn and Pb).

2.4.Eutrophication potential calculations

The eutrophication potential(E)of biogas slurry was calculated using the modified green degree method[38].The formula for calculating theEof biogas slurry samples is as follows:

2.5.Risk assessment

The toxicity of heavy metals in the biogas slurry samples were evaluated using the contamination degree (Cd) and potential ecological risk index (RI),which were acquired using H?kanson approach [40,41].Cdand RI were defined as follows:

Whereiincludes seven heavy metals in biogas slurry,namely As,Cd,Cr,Cu,Hg,Pb and Zn;is the contamination factor of metali;is the average content of metaliin biogas slurry,μg?L-1;is the standard preindustrial reference level of metali,μg?L-1;Cdis the contamination degree of biogas slurry;is the potential ecological risk factor of metali;is the ‘‘toxic-response”factor of metali.RI is the requested potential ecological risk index of biogas slurry.The standard preindustrial reference level and ‘‘toxicresponse”factors of the seven heavy metals are shown in Table S2 [41].Since H?kanson approach was previously used to evaluate the potential ecological risk of sediments,the standard preindustrial reference level was based on the preindustrial sediments [42].We selected Directive 98/83/EC as the standard preindustrial reference level of biogas slurry,and promoted H?kanson approach to evaluate the potential ecological risk of biogas slurry.Table 2 shows the terms are used to describe theand RI[41].

Table 2 The terms are used to describe the and RI [37]

Table 2 The terms are used to describe the and RI [37]

3.Results and Discussion

3.1.COD,-N and anions analyses

The total amount of COD in all biogas slurry samples ranged from 315 mg?L-1to 18,170 mg?L-1.Only one COD concentration of the biogas slurry sample from Lanzhou was >10,000 mg?L-1,and the COD concentration of the six biogas slurry samples were<1000 mg?L-1,among which five used SM as the digester raw material.The maximum COD average concentration from biogas slurry samples of CHM raw material was up to 7092 mg?L-1.

Table 3 Concentration of COD,-N,anions and COD/ ratio in biogas slurry samples

Table 3 Concentration of COD,-N,anions and COD/ ratio in biogas slurry samples

Table 3 also shows that the Cl-concentration of biogas slurry varied from 5.84 mg?L-1to 232.17 mg?L-1.The two biogas slurry samples with the Cl-concentration beyond 100 mg?L-1used KW as the digester raw material.However,No.21 biogas slurry sample,which also used KW raw material,had the lowest Cl-concentration.This result may be due to the abundant NaCl in KW.Moreover,the amount of NaCl added was relatively varying in different foods.The Cl-concentration variance from KW digesters was relatively large.

3.2.Eutrophication potential

Fig.1 shows the eutrophication potential of biogas slurry from the biogas plants of five raw materials.The detailed eutrophication potential of 31 biogas slurry samples is shown in Fig.S1 (see Supplementary Material ).Among the three components of eutrophication potential,ENandEPwere considered as the main sources of the eutrophication potential in biogas slurry,while the proportion ofECODwas the least.Since the concentrations of COD,-N andin biogas slurry samples from CHM raw material were significantly higher than those of other raw materials,the eutrophication potential of biogas slurry from CHM raw material was the lowest,manifesting the most serious eutrophication threat.On the other hand,it demonstrated that the biogas slurry with chicken manure as raw material has abundant nutrient content and is the most suitable for agricultural fertilizer.The eutrophication potential of biogas slurry from CAM raw material was the highest,indicating that the biogas slurry from CAM raw material presents the least eutrophication threat.

Fig.1.Eutrophication potential of biogas slurry from five raw materials.

3.3.Antibiotics analyses

The six classes of antibiotic concentration,namely sulphonamides,quinolones,β2-receptor agonists,macrolides,tetracyclines and crystal violet,in biogas slurry samples are shown in Fig.2.Sulphonamides,quinolones and tetracyclines were detected with the highest concentration levels in biogas slurry samples from SM raw material,116.19 μg?L-1,324.34 μg?L-1and 150.27 μg?L-1respectively.The high sulphonamide,quinolone and tetracyclines concentration indicated that they were the most frequently used antibiotics in swine feeding.By contrast,the antibiotic concentration was detected with low concentration level in biogas slurry samples from CAM,which was significantly lower than those of other materials.Quinolones,macrolides and tetracyclines were detectable in biogas slurry samples from five raw materials.Sulphonamides were detectable in biogas slurry samples from SM,KW and CHM.Few β2-receptor agonists and crystal violet were detected.

Many antibiotics are frequently used as animal feed additives,but they are hardly absorbed by the animals,leading to the excretion of 30%–90% of the antibiotics via faeces or urine [51,52].In general,the species and sizes of animals differ in the variety and dosage of antibiotics [32,53–55].Accordingly,the antibiotic content in biogas slurry varies with the types of animals and antibiotics.

Antibiotics cause not only environment pollution,but also inhibition the anaerobic digestion process and disadvantageous to biogas production.Lallaiet al.[56] and Shiet al.[57] researched the influence of antibiotics on biogas production using SM as the digester raw material.The results indicated that microbic activity is inhibited by antibiotics,thereby leading to defer initial time of biogas generated and low daily CH4production.

Among these antibiotics,sulphonamides,quinolones,macrolides and tetracyclines in biogas slurry samples from different districts and different raw materials are shown in Figs.S2–S5.

Sulphonamides are found in biogas slurry samples from SM,KW and CHM.Seventeen types of sulphonamides were detected (as shown in Table S3).Sulfamonomethoxine,sulfamethazine,sulfaisodimidine,sulfacetamide and sulfamethoxypyridazine were detected with high concentration levels.The sulphonamide distribution in biogas slurry samples are shown in Fig.S2.The sulphonamides concentration of biogas slurry from SM was found to be significantly higher than that of biogas slurry from other raw materials.Sulphonamide antibiotics are frequently used in swine farm to promote growth and treat swine disease,such as toxoplasmosis,swine dysentery and swine plague,resulting in sulphonamide antibiotics residues in SM [33].The sulphonamide contents of the biogas slurry samples from SM contained sulfamonomethoxine(17.4%),sulfamethazine (44.8%),sulfamethoxypyridazine (11.5%)and sulfaisodimidine (25.7%).

Nine types of quinolones were detected in this study(as shown in Table S4),but three of which (i.e.norfloxacin,danofloxacin and sarafloxacin) were below the limits of detection.The other six types of quinolones are presented in Fig.S3,wherein quinolones in biogas slurry samples were almost mainly marbofloxacin,with two exceptions (Nos.21 and 31).Marbofloxacin in biogas slurry samples from SM raw material was up to 324.08 μg?L-1and much higher than the biogas slurry from other raw materials.Marbofloxacin is used in the treatment of swine respiratory disease,and has an effective bactericidal effect onActinobacillus pleuropneumoniaeandPasteurella multocida[58].

Macrolides were found in a fraction of biogas slurry samples.Four types of macrolides were detected in this study (as shown in Table S5).The macrolide contents are shown in Fig.S4.Macrolides were detected in more than half of biogas slurry samples.The macrolides in the biogas slurry samples were almost mostly lincomycin,except for No.31.Lincomycin could be analysed in No.20 biogas slurry samples from KW raw material with a maximum concentration of 71.34 μg?L-1.Lincomycin is a wellestablished antibiotic drug used in human and veterinary medicine,which is conducive to cure the infection caused by Grampositive pathogens.Therefore,lincomycin is widely used in swine,cattle and poultry industry.To make matters worse,the risk of lincomycin residues presents in food products [59].

Fig.2.Six classes of antibiotic concentration of biogas slurry samples from different districts and different raw materials.

Tetracyclines were found in most biogas slurry samples.Four types of tetracyclines were detected in this study (as shown in Table S6),but only small chromatographic responses were determined in the case of chlortetracycline,indicating that the chlortetracycline concentration was below the limits of detection.The contents of the other three types of tetracyclines (i.e.oxytetracycline,tetracycline and doxycycline)are shown in Fig.S5.Oxytetracycline was detected with a significantly high content in tetracyclines for all raw materials.The oxytetracycline proportion is 82.1%,94.9%,100%,62.1%and 51.3%for the biogas slurry samples with CAM,SM,St+M,KW and CHM as raw material,respectively.Oxytetracycline is a broad-spectrum antibiotic used to treat swine bacterial diseases via intramuscular injection or in feed,leading to oxytetracycline residues in SM [60].Hence,the oxytetracycline concentration of biogas slurry samples from SM raw materials is significantly higher than other raw materials.

3.4.Heavy metals and potential ecological risk assessment

The concentration of seven heavy metals in biogas slurry samples from the different districts and different raw materials are shown in Table 4.Zn concentration in biogas slurry samples was dramatically higher than the concentration of other six heavy metals.The As average concentration in biogas slurry samples from kitchen waste is the highest among the five raw materials,reaching up to 122.26 μg?L-1.Obviously,on account of the different order of magnitudes from various types of heavy metals,the total heavy metals concentration of biogas slurry cannot availably evaluate their risk on the environment [1,3,4,61].To quantitatively express the toxicity of heavy metals,theCdand RI were calculated using H?kanson approach.

Table 4 Concentration of heavy metals in biogas slurry samples

Table 5 The parameters of quadratic polynomial stepwise regression model

Fig.3.Contamination factors and contamination degree of biogas slurry from different raw materials.

Fig.4.Risk factors and risk indices of biogas slurry from different raw materials.

3.5.Quadratic polynomial stepwise regression model set up

The quadratic polynomial stepwise regression model was established to quantitatively describe the correlation among-N,and heavy metal concentrations in the biogas slurry samples(Eq.(6)).

WhereYiis the calculated concentration of metali,μg?L-1;XNis the-N concentration in biogas slurry,mg?L-1;XPis theconcentration in biogas slurry,mg?L-1;β0–β5are the model parameters(Table 5).

Fig.5 shows the comparisons between experimental concentration and calculated concentration of the seven heavy metals in biogas slurry samples.All sevenRvalues exceeded 0.8,showing a highly acceptable correlation.When the concentrations of As,Cd,Cr,Cu,Hg,Pb and Zn were below 120 μg?L-1,2.2 μg?L-1,80 μg?L-1,400 μg?L-1,2.0 μg?L-1,12 μg?L-1and 1500 μg?L-1,respectively,the quadratic polynomial stepwise regression model can quantitatively describe the correlation among-N,and heavy metals concentration of biogas slurry.The results provide a model basis for the treatment and control of-N,and heavy metals in biogas slurry.

4.Conclusions

(1) The COD concentration in biogas slurry samples from SM was lower than those in the other four types of raw materials.The COD,-N andconcentration were the highest in biogas slurry samples from CHM,which indicated the most serious eutrophication threat.The Cl-concentration was the highest in the biogas slurry samples from KW.The C/N ratios of the biogas slurry samples from the five raw materials were <10.

(2) Antibiotics are generally detected in biogas slurry samples.The concentration of three types of antibiotics(i.e.sulphonamides,quinolones and tetracylines)in the biogas slurry from SM was much higher than the other types.The quinolone concentration in the biogas slurry from SM,St+M and CHM were excessively high.The five types of raw materials contained a certain amount of tetracylines in biogas slurry.

(3) TheRIlevel showed that biogas slurry had a moderate potential ecological risk,except for the biogas slurry from CAM.This result indicated that a potential threat from biogas slurry was universal.The potential ecological risks of As and Hg were particularly high.

(4) The quadratic polynomial stepwise regression model can quantitatively describe the correlation among-N,and heavy metals concentration of biogas slurry from the biogas plants.

Fig.5.Comparisons of experimental and calculated As (a),Cd (b),Cr (c),Cu (d),Hg (e),Pb (f) and Zn (g) concentration of biogas slurry.

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.

Acknowledgements

This work was supported by the National Natural Science Foundation of China(22038012,42077030),the Science and Technology Program of Fujian Province,China (2020NZ012015,2020Y4002)and the Fundamental Research Funds for the Central Universities of China (20720190001).

Supplementary Material

Supplementary data to this article can be found online at https://doi.org/10.1016/j.cjche.2021.05.039.