Research Article

pubs.acs.org/journal/ascecg

Coupling Hydrothermal Treatment with Stripping Technology for

Fast Ammonia Release and Eective Nitrogen Recovery from
Chicken Manure
Weiwei Huang,, Tian Yuan,, Ziwen Zhao, Xi Yang, Wenli Huang, Zhenya Zhang,*,
and Zhongfang Lei*,

Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan
MOE Key Laboratory of Pollution Process and Environmental Criteria, College of Environmental Science and Engineering, Nankai
University, No. 94 Weijin Road, Nankai District, Tianjin 300071, China

S Supporting Information
*

ABSTRACT: In order to mitigate the environmental impacts

associated with accelerated global N cycle, a hybrid pretreatment
procedure combining hydrothermal treatment (HTT) with
ammonia stripping was developed to eectively recover N as a
valuable ammonia product from chicken manure (CM).
Processing of the CM at 180 C for 30 min resulted in a
208% increase in soluble organic carbon (SOC) and 46%
conversion of organic-N to ammonia-N. Analysis of carbon mass
balance revealed that carbohydrates, proteins, and volatile fatty
acids (VFAs) were the major contributors to SOC (100%) in
the processed CM under this HTT condition. Further
prolongation of holding time to 60 min or increase of HTT
temperature to 220 C resulted in some increase in ammonia
yield but obvious decrease in SOC concentration and possible
formation of inhibitory or nonbiodegradable products as well, compromising the practical value of the processed CM as
feedstock for methane production. After ammonia recovery through a circulating stripping system coupled with acid absorption,
methane production potentials of the resultant ammonia-stripped CM residue were assessed via 45 days anaerobic digestion
trials. Results from this work reected an overall N recovery eciency of 57% from CM and increase in methane yield by 24%
(compared to those of raw CM).
KEYWORDS: Ammonia stripping, Chicken manure, Hydrothermal pretreatment, Soluble organic products, Methane

INTRODUCTION
Ammonia that is produced primarily through the Baber-Bosch
reaction is an important raw material in the chemical industry.
Also, it is regarded as a promising H2 energy carrier due to its
high H density, CO2 free nature, and easy long-distance
transportation.1 Nevertheless, the xation and application of
massive amounts of ammonia has disturbed and accelerated the
global N cycle, leading to a wide range of environmental
problems.2 The conicts between environmental preservation
and the need for development have propelled us to seek
alternatives for ammonia production in a renewable and
sustainable way.
Animal manure represents one of the biggest anthropologic
sources of N pollution. Traditionally, it has been disposed of in
farmlands to improve soil fertility, but in recent decades, this
practice is handicapped by the availability of low cost chemical
fertilizers. The N nutrients in animal manure are often not used
to their potential, which poses a burden to the environment
and leads to an imbalance of N nutrients. Therefore, there is a
clear demand for N recycling from the organic manure so that
XXXX American Chemical Society

the environmental problems can be alleviated, and the

accelerated global N cycle can be halted.
In this study, chicken manure (CM) typically with a high
organic-N content was selected as an example of animal
manure. To achieve eective recovery of N from CM as
ammonia, the primary step is to nd an ecient method to
disintegrate the organic N. Recently, hydrothermal treatment
(HTT) has been recognized as an appealing approach for
organic solid degradation, with potential benets of reclaiming
various useful products like reducing sugars,3 volatile fatty acids
(VFAs),4 phosphorus,5,6 and energy.710 Although ammonia
has been identied as the major mineral product from HTT
degradation of N-containing compounds,1114 its recovery has,
however, not received much attention. A previous work11 on
hydrothermal deamination of sewage sludge has identied three
characteristic hydrothermal regimes: hydrolysis of labile protein
Received: February 13, 2016
Revised: May 16, 2016

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX

Research Article

ACS Sustainable Chemistry & Engineering

and inorganic-N compounds below 300 C, pyridine-N
deamination at 340 C, and stable protein deamination at
380 C. A signicant N reduction by 76.9% in the solid residue
was observed at 380 C.11 Despite the ecient ammonia
release at this high temperature, the cost for heating and device
setup remains a challenge. An alternative is thus directed
toward the degradation of organic-N at milder HTT temperatures 220 C, within which range labile organic-N can be
partially destructed without intensive formation of polycyclic
aromatic hydrocarbons or pyridine-N restricting the ammonia
release eciency and compromising digestibility of the CM
residues.9,10,15,16 However, no systematic and elaborate
information can be found on either the mechanisms of
ammonia release at this temperature range or the dynamic
interactions between ammonia release and organic-C solubilization. Thus, an elaborated understanding of the conversion
from organic-N to ammonia is prerequisite for optimization of
the HTT process to achieve high and economical ammonia
release eciency and maximum utilization of the solid residue
for energy production. The produced ammonia can be
recovered by stripping technology, an eective process that
can be applied for ammonia recovery from dry anaerobic
digested swine manure as proven recently by Huang et al.17
The HTT processed and ammonia-stripped CM residue can
serve as ideal feedstock for anaerobic digestion (AD).
The objective of this work was to nd out the proper HTT
conditions to achieve fast and ecient ammonia release from
CM. To make full use of CM, attention was also paid to the
accumulation of other useful organic products including soluble
proteins, carbohydrates, and VFAs. More specically, during
the HTT process the eects of temperature and holding time
on organic solids solubilization and ammonia release were
elucidated. Furthermore, the potential of ammonia-stripped
CM for methane (CH4) production was tested via AD trials
after ammonia was recovered by a circulating stripping system
developed in the laboratory.

Table 1. Characteristics of Raw Chicken Manure and

Anaerobic Sludge Used in the Experimentsa
raw chicken
manure (RCM)

anaerobic sludge
(seed sludge)

41.99 (1.40)

5.31 (0.13)

24.53 (0.78)

4.06 (0.11)

mg/g-VS

10.15 (0.53)

6.97 (0.16)

mg/g-VS
mg/g-VS

34.23 (1.70)
33.55 (1.79)

64.45 (3.17)
62.18 (2.31)

mg/g-VS

23.40

55.21

6.08 (0.14)
9.30 (0.13)

7.28 (0.17)
5.84 (0.10)

general property
total solids (TS, wet
weight based)
volatile solids (VS, wet
weight based)
total ammonia nitrogen
(TAN)
total nitrogen (TN)
total Kjeldahl nitrogen
(TKN)
total organic nitrogen
(TON)b
pH
C/N

unit

Note: pH of RCM was determined in the diluted manure samples

with TS content of 25%. The data are expressed as mean (SD) values
of ve tests. bTON = TKN TAN.

was dened in this work as the elapsed time from the moment when
the reactor rst reached the preset temperature to that when the
cooling started. The corresponding pressures at 140, 180, and 220 C
were 0.3, 1.0, and 2.7 MPa, respectively.
Ammonia Recovery. Ammonia stripping from the HTT
processed CM was carried out in an enclosed and circulating system
as described in a previous work.17 The experimental stripping setup
consisted of a set of 500 mL containers. Pretreated CM (100 g; wet
weight) was loaded into the stripping bottle equipped with a stirring
device, and the headspace of the system was ushed with N2 to
maintain an anaerobic environment. The gas was rst humidied by
the water containing bottle and then purged through the manure
containing bottle placed in a water bath at a gas ow rate of 170 mL/
min. The escaped ammonia was absorbed by a 1.5 M HCl solution.
This stripping system has been previously tested to be successful for
ammonia recovery from fermented swine manure at 20% TS.17 On the
basis of the previous results, ammonia stripping from the HTT
processed CM was conducted at initial pH 11.0 (adjusted with
Ca(OH)2) and 55 C for 3 h in this study.
Methane Fermentation. For CH4 fermentation, the test
fermenter, a 500 mL glass bottle, was loaded with 80 g of RCM
(adjusted with deionized water to 25% TS) or the ammonia-stripped
CM together with 150 g of seed sludge and 170 g of deionized water.
Meanwhile, the control reactor was loaded with the same amount of
seed sludge and added with deionized water to achieve a nal volume
of 400 mL. System pH was adjusted to around 7.0 with 1.5 M HCl
solution. After thoroughly mixing, the bottles were then sealed with
rubber stoppers, ushed with N2, and incubated at 35 C in an
incubator. Each fermentation experiment was conducted in duplicate.
The CH4 production potential of CM, presented as milliliter of (CH4)
per gram of CM volatile solids (mL/g-CMVS), was corrected by
subtracting the CH4 yield obtained from the control reactors.
Analytical Methods. The owchart of sample analysis during
HTT experiments is illustrated in Scheme S1 (Supporting
Information). After the reactor was cooled down to room temperature,
the headspace gas was released and collected by a gas sampling bag
(Tedlar bag, Asone). Then, the collected gas was scrubbed by HCl
solutions (1.5 M, 500 mL 2) in a sealed and circulating stripping
system for 35 min at a gas ow rate of 170 mL/min to guarantee
complete capture of the gaseous ammonia. The stripping system
(scrubbing bottles, tubes, and gas pump) was ushed with N2 before
the experiment. Finally, carbon dioxide (CO2) content in the acidscrubbed gas was analyzed by a Shimadzu GC-8A/TCD packed with a
Porapak Q column, and the gas volume was quantied by water
displacement. The whole procedure was conducted in a sealed
environment.
For solid samples analysis, the HTT processed CM was collected
carefully and weighted for total weight loss. Contents of TS and

MATERIALS AND METHODS

Raw Materials. Raw chicken manure (RCM) was collected from a

local farm (Ibaraki, Japan) and stored at 4 C before use. Mesophilic
anaerobic sludge was sampled from a wastewater treatment plant in
Ibaraki, Japan, and used within 24 h. The sludge was concentrated by
centrifugation at 7300g for 10 min and used as seed sludge for CH4
fermentation after the supernatant was discarded. Characteristics of
the raw materials are listed in Table 1.
Hydrothermal Treatment Experiments. The HTT experiments
were performed in a 200 mL enclosed stainless steel reactor equipped
with a cylindrical electric heater and an internal temperature sensor
(OM Lab-tech MMJ-200, Japan). Temperatures were maintained
within 6 C of set conditions. Agitation was realized by a motor-driven
propeller throughout the experiments. A 130 g mixture of RCM and
deionized water was loaded into the reactor with total solids (TS)
content being adjusted to around 25% according to the preliminary
trials. A total of 12 HTT conditions were tested, and each condition
was repeated three times. Under a constant agitation rate of 100 rpm,
the reactor was heated up to the preset temperature (140 C, 180 C,
or 220 C), and then the reactor was maintained at this temperature
for a designated time duration (0, 15, 30, or 60 min). At the end of the
HTT experiment, the heater was powered o, and the reactor was
cooled with a fan to room temperature (around 25 C) before further
analysis. Figure S1 (Supporting Information) illustrates the temperature change in the reactor under dierent HTT conditions. The
reactor temperature was elevated at an average rate of 14.4, 12.1, and
11.4 C/min during the heating process when the designated
temperature was 140, 180, and 220 C, respectively. Holding time
B

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX

Research Article

ACS Sustainable Chemistry & Engineering

volatile solids (VS) were determined before and after the HTT
experiments. The TS was determined as the constant dry matter (DM)
remaining in the manure samples after drying at 105 C for 24 h, and
VS was calculated as the loss of DM after burning at 600 C for 3 h.
Contents of organic C, H, and N in the DM were determined by an
organic elemental analyzer (PerkinElmer 2004 CHN, USA). Manure
pH was measured directly using a semisolid pH meter (Testo 206,
Germany). For analysis of total nitrogen (TN) and total Kjeldahl
nitrogen (TKN), the solid manure was diluted and mixed with a
known amount of deionized water and then measured in accordance
with standard methods.18 Total organic nitrogen (TON) was
calculated as the dierence between TKN and total ammonia nitrogen
(TAN).
As indicated in Scheme S1, samples for the measurement of soluble
products were prepared by diluting 4 g of manure (wet weight) with
40 mL of deionized water. The resultant mixture was then centrifuged
at 7300g for 20 min, and then, the resultant supernatant was ltered
through 0.45 m membrane (PTFE, Membrane Solutions, US).
Ammonia-N in the ltrate was determined according to standard
methods.18 Concentration of TAN in the HTT processed CM was
recorded as the sum of ammonia-N detected in the ltrate and the
amount that escaped from the reactor and absorbed by the scrubbing
solutions. Concentrations of VFAs were determined via Shimadzu GC14B/FID equipped with a Unisole F-200 30/60 column (Japan).
Soluble organic carbon (SOC) was analyzed by a TOC analyzer
(Shimadzu TOC-VCSN, Japan). Carbohydrates and proteins were
measured with the phenol-sulfuric method19 and the Coomassie
brilliant blue method,20 respectively.
Biogas production was measured and calculated according to
readings on the scale of syringes connected to the fermentation
bottles. The content of CH4 was determined by Shimadzu GC-8A
(Japan).
Calculation. Reduction in TS (%) or VS (%) after the CM being
hydrothermally treated was dened as follows:
TS reduction(%) =

[initial TS] [final TS]

100
[initial TS]

(1)

VS reduction(%) =

[initial VS] [final VS]

100
[initial VS]

(2)

repetitions. For each fermentation experiment, the CH4 yield was

calculated according to the results obtained from the two parallel
fermentation trials. The analysis of statistics and correlation
coecients was performed by using SPSS statistics 19.0 (IBM,
Armonk, NY, USA). Signicance was assumed at p < 0.05.

RESULTS AND DISCUSSION

Reduction of TS and VS after HTT. Figure 1 indicates the
reductions in TS and VS after HTT. The TS and VS contents

Figure 1. Reductions in total solids (TS) and volatile solids (VS) after
the hydrothermal treatment (HTT) process.

of CM decreased in all scenarios. An increase in temperature

apparently resulted in accelerated disintegration of organic
substances, contributing to higher TS and VS reduction
eciencies in the processed CM. The greatest levels of
reduction in both TS and VS were observed at 220 C.
Figure 1 also shows that longer treatment duration favored
the solids dissolution to some extent, especially at 220 C
during the initial 15 min. After HTT at 220 C for 060 min,
the reductions in TS and VS varied between 17.64%24.65%
and 25.36%28.77%, respectively. In all tested scenarios,
increased temperature rather than prolonged holding time
seemed to exert a greater inuence on TS and VS reductions.
Solubilization of Solid Organics during HTT. As shown
in Figure 2a, after HTT at 140 C for 060 min, the soluble
proteins in the processed CM remained relatively stable with
variations in concentration less than 20% compared to that of
RCM. However, it was remarkably accumulated to 137.33 mg/
g-VS as HTT temperature increased to 180 C (for holding 15
min), while it signicantly decreased to 25.33 mg/g-VS when
HTT was conducted at 220 C holding for 60 min. After HTT
at 180 C for 060 min, the concentration of carbohydrates
was increased by about 200%600% relative to RCM. The
highest level of carbohydrates was recorded as 416.08 mg/g-VS
after HTT at 180 C for 30 min. It was observed that
prolongation of reaction time to 60 min or further increasing
HTT temperature to 220 C led to a dramatic decline of
carbohydrate concentration, similar to the trend detected in
protein concentration.
Compared to the changes of carbohydrates and proteins, the
total volatile fatty acids (TVFAs) remained relatively stable in
the processed CM at each HTT temperature when this
pretreatment process lasted for 060 min (Figure 2b). More

To study the decomposition eciency of organic-N to ammonia-N,

N mass balance was also analyzed. In this study, TAN yield (mg/g-VS)
was dened as the net increase of TAN in CM after HTT (i.e., [nal
TAN] [initial TAN]). N recovery eciency was calculated
according to eq 3.

N recovery efficiency (%) =

TAN release (mg)

100
loss of organic N (mg)

(3)
in which TAN release (mg) = [TAN yield] (mg/g-VS) VS (g), and
the loss of organic-N is the dierence of organic-N in CM samples
before and after HTT.
Conversion ratio of TON to TAN (%), nal TAN/TKN ratio (%),
and volumetric TAN yield (g/L) dened, respectively, by eqs 4, 5, and
6, were used in this study to compare the performance of ammonia
release from manure wastes through dierent treatment methods.

Conversion ratio of TON to TAN (%) =

[TAN yield]
100
[initial TON]
(4)

Final TAN/TKN ratio (%) =

[final TAN]
100
[final TKN]

Volumetric TAN yield (g/L) = [TAN yield] [VSconc ]

(5)
(6)

where VSconc is in g/L.

Statistical Analysis. For each HTT condition, three replicates
were conducted, and the determination of related parameters was
duplicated. All of the results are expressed as the mean values of six
C

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX

Research Article

ACS Sustainable Chemistry & Engineering

Figure 2. Proles of (a) soluble proteins and carbohydrates, (b) volatile fatty acids (VFAs) including acetic acid (HAc), propionic acid (HPr), nbutyric acid (n-HBu), and iso-valeric acid (iso-HVa), (c) soluble organic carbon (SOC) and its major contributors in the treated chicken manure,
and (d) CO2 production during HTT.

VFAs were found to accumulate during HTT at 220 C, and

acetic acid (HAc) was the dominant component in all trials
(>80%). Interestingly, HAc was the sole VFA component in all
HTT processed CM samples at 140 C and in RCM, and
propionic acid (HPr) was detectable when HTT was carried
out at 180 C when holding longer than 15 min or at 220 C.
The concentrations of n-butyric acid (n-HBu) and iso-valeric
acid (iso-HVa) were found to be much less, about 1.73 mg/gVS and 1.10 mg/g-VS only after HTT at 220 C and holding
for 30 and 60 min, respectively.
Concentrations of SOC in the raw and the processed CM
samples are depicted in Figure 2c. Obviously, the SOC
increased in all of the treated samples in comparison to that
in RCM. Temperature had a profound inuence on SOC. An
increase in HTT temperature from 140 to 180 C favored the
dissolution of carbonaceous organics from CM. Further
increase in temperature from 180 to 220 C, however, resulted
in decreased SOC most probably due to the breakdown of
soluble organic matter into gaseous or mineralization products.
Holding time also inuenced the concentration of SOC to

some extent, especially at 180 C. The highest SOC level,

243.11 mg/g-VS, was detected in the CM samples treated at
180 C for 30 min, while the SOC concentration was found to
decrease to 211.30 mg/g-VS when holding time was prolonged
to 60 min at this temperature.
In order to study the percentage distribution of carbohydrates-C, proteins-C, and TVFAs-C in SOC, carbon mass
balance was also analyzed in this work as illustrated in Figure
2c. The C content of proteins was estimated based on a
theoretical formula (C4H6.1O1.2N),21 while that of carbohydrates was based on glucose (C6H12O6). In addition, the
calculation of TVFA-C was based on the individual VFA. As
shown, the smallest dierences, 0.9% and 1.4% between the
measured SOC and calculated organic-C in terms of soluble
proteins, soluble carbohydrates, and TVFAs, were obtained
from the samples treated at 180 C for 15 and 30 min,
respectively, apparently indicating that carbohydrates-C,
proteins-C, and TVFAs-C were the major components of
soluble organics in the processed CM under these two HTT
conditions. The larger gap found between the measured SOC
D

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX

Research Article

ACS Sustainable Chemistry & Engineering

and calculated organic-C at a higher temperature of 220 C was
probably attributable to the generation of smaller molecular
weight organic compounds (e.g., amino acids, lactic acids,
alcohols, etc.)14,15 or melanoidins16 occurred during the
hydrolysis step of HTT or through the reaction between
carbohydrates and amino groups coexisting in the CM. Further
characterization and identication of the produced organics are
necessary to shed light on this complicated HTT process.
Gaseous Products during HTT. Gas analysis conrmed
the formation of CO2 in the headspace of the HTT reactor as
shown in Figure 2d. An increase in both temperature and
holding time favored the generation of CO2, which occurred
primarily via decarboxylation7 and was identied as the
predominant C-source gas at HTT temperatures 220 C.8
As noticed, the generation of CO2 was negligible at 140 C,
while it started to evolve quickly and increased along with the
duration of the HTT process at 180 C. When HTT was
conducted at 220 C, the evolution of CO2 became remarkably
evident, ranging between 53.7861.52 mL/g-VS when this
pretreatment lasted for 060 min. The CO2 evolution under
HTT at 220 C was to some extent in agreement with the
decrease in SOC concentration (Figure 2c).
Changes in Ammonia Concentration and System pH.
Figure 3a depicts the eects of dierent HTT conditions on pH
variation and TAN release from the CM. As shown, increase in
both temperature and holding time was favorable for TAN
release (except HTT at 220 C for 060 min). The production
of TAN reached a maximum of 22.85 mg/g-VS after HTT at
180 C for 60 min, corresponding to a TON conversion ratio
of 54.4%. Further increase in temperature to 220 C led to an
insignicant increase in TAN concentration (p = 0.544 > 0.05),
although further reduction in TS or VS was observed at 220 C
(Figure 1). Three reasons might be accountable for this
phenomenon. First, uric acids with a high N content
(approximately 33%, calculated based on its formula,
C5H4N4O3) and low molecular weight could undergo thermal
breakdown to form ammonia easily at 140 and 180 C, while
intense decomposition of macromolecular proteins with
typically lower N content of about 16% according to their
theoretical formula (C4H6.1O1.2N)n21 usually occurs at higher
temperatures. Second, the majority of labile organic-N in CM
could be degraded at temperatures lower than 220 C, while
thermal destruction of the single amino acids formed or the rest
of the stable proteins may require higher activation energy.11 In
addition, hydrothermal decomposition of organic-N to form
ammonia might be limited at 220 C due to the polymerization
of amino groups into melanoidins, whereas great weight loss of
organic CM was observed as the temperature increased from
180 to 220 C (Figure 1). Given the complexity of
hydrothermal reactions and chemical components in CM,
further investigation on the dynamic interactions between
various factors is necessary to make clear the mechanisms
underlying this phenomenon.
The fraction of gaseous ammonia-N entrapped by the
scrubbing solution is demonstrated in Figure 3b. Clearly,
although an increasing trend was detected in the gaseous
ammonia-N with the increase in HTT temperature and holding
time, the amount was negligible when compared to that of
TAN (Figure 3a).
The manure pH varied most probably as a result of the
dynamic interaction between ammonia release and organic acid
production. During HTT at 140 C, fast ammonia release led
to increased system pH from 6.08 to 7.177.41. When more

Figure 3. Eects of hydrothermal treatment (HTT) on (a) total

ammonia nitrogen (TAN) release and pH variation (where NS
indicates no signicant dierence, *p < 0.05 according to Duncans
multiple range tests), and (b) the production of gaseous ammonia-N.

pronounced accumulation of organic acids (e.g., VFAs, etc.)

occurred at 180 and 220 C (Figure 2b), the system pH was
detected to decline to be around or even below 7.00.
Organic-N Decomposition and N Mass Balance. The
variations of organic C, H, and N contents in the solid fraction
of raw and processed CM were investigated and presented in
Figure 4 in terms of H/N ratio and C/N ratio. As shown, both
H/N and C/N ratios decreased in all of the treated CM in
comparison to those of RCM. On the whole, an increase in
temperature led to higher mineralization eciency of organic-H
and organic-C than organic-N in the CM. This observation
might be brought about by the following reasons: (1) the
condensation of amino groups through the Maillard reaction
may restrict organic-N mineralization; (2) accelerated decarboxylation of the organic matter in CM at increasing HTT
temperatures; and (3) higher temperatures above a certain level
might be prerequisite for the cleavage of stable proteins
remaining in the particulate substances (CM in this study).11
Besides the eects of temperature and holding time on
organic-N mineralization during the HTT process, other factors
like raw material compositions, system pH, water content, and
coexisting ionic compounds including phosphorus, magnesium,
calcium, etc. might also contribute to the retardation of
E

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX

Research Article

ACS Sustainable Chemistry & Engineering

Increasing holding time from 30 to 60 min at 180 C led to a

small increase in TAN concentration (p = 0.069 > 0.05) but an
undesirable decline of soluble proteins and carbohydrates
concentration by 38.5% and 26.0%, respectively, compromising
subsequent utilization of the CM residues. Considering the
energy consumption associated with temperature and reaction
time, energy eciency for ammonia release, and accumulation
of useful organic products for their possible reclamation or
boosting CH4 fermentation, the optimum HTT operational
conditions in this study were determined to be 180 C for
holding 30 min.
Comparative Study on Ammonia Production and
Correlation Analysis Between Dierent Tested Parameters. Table 2 lists the performances of dierent treatment
methods on ammonia release from manure wastes. Among
these treatment methods, HTT is an advantageous option
owing to its eectiveness, no need of chemicals addition,
relatively short reaction time, and low water requirement.
Temperature is a crucial factor governing the extent to which
TON conversion can proceed. As seen from Table 2, high TS
content CM (25% TS in this study) can be processed in HTT
systems, yielding higher volumetric TAN production with
smaller reactor volume.
Table S2 (Supporting Information) displays the result of
correlation analysis between the tested parameters after HTT
of CM under the 12 designed conditions. As indicated, the nal
TAN concentration in the processed CM had signicantly
positive correlations with TS and VS reduction, VFAs
production, and CO2 generation (p < 0.01), implying that
ammonia-N is generated concomitantly with the destruction of
solid organic matter into smaller molecular weight compounds.
Ammonia Recovery from HTT Processed CM by
Stripping. Ammonia stripping was carried out with the four
processed CM samples: HTT180-15, HTT180-30, HTT18060, and HTT220-0 due to their relatively higher TAN yields
(Figure 3a and Table 2). After 3 h of stripping in the circulating
system, the ammonia-N removal eciencies of the four samples

Figure 4. Changes in ratios of organic C/N and H/N in the solid

residue of hydrothermal processed chicken manure.

ammonia-N release at higher temperatures in this study. The

synergetic eects of these multiple factors on ammonia
production during HTT of CM are also necessary for future
investigation.
Table S1 (Supporting Information) summarizes the N mass
balance analysis under four typical HTT conditions: (1) HTT
at 180 C holding for 15 min (HTT180-15), (2) HTT at 180
C holding for 30 min (HTT180-30), (3) HTT at 180 C
holding for 60 min (HTT180-60), and (4) HTT at 220 C
holding for 0 min (HTT220-0). During the HTT process, the
DM content decreased mainly because of the formation of
water and gaseous products. High N recovery eciencies in the
range of 82.40% to 89.02% were achieved under the four typical
scenarios, signaling that ammonia-N was the main product
during the mineralization of organic-N when the HTT process
was performed at 180220 C.

Table 2. Comparison of Ammonia Release Eciencies Obtained through Dierent Treatment Methodsa
TON conversion to TANb

initial substrate characteristics

treatment
method

operation conditions

manure

TS
(%)

VS
(%)

TKN
(mg/g-VS)

TON
(mg/g-VS)

ratio
(%)

TAN/
TKN (%)

volumetric TAN
yield (g/L)

refs

hydrothermal

180 C for 15 min

chicken

25.0

14.6

33.55

23.40

42.2

59.7

1.44

hydrothermal

180 C for 30 min

chicken

25.0

14.6

33.55

23.40

46.4

62.6

1.59

hydrothermal

220 C for 0 min

chicken

25.0

14.6

33.55

23.40

58.3

70.9

1.99

thermo-alkaline

120 C for 30 min,

0.07g/g-TS NaOH
120 C for 30 min,
0.07g/g-TS CaO
120 C for 30 min, 2%
(V/V) H2SO4
120 C for 30 min, 0.74%
(V/V) HCl
specic energy input: 500
kJ/kg-TS
65 C for 8 days at initial pH
8.5
55 C for 8 days at initial pH
10.0

dairy

6.7

5.8

33.77

27.61

12.1

28.1

0.20

this
work
this
work
this
work
22

dairy

6.7

5.8

33.77

27.61

13.1

28.9

0.21

22

dairy

6.7

5.8

33.77

27.61

17.1

32.2

0.28

22

dairy

6.7

5.8

33.77

27.61

16.6

31.8

0.27

22

hog

9.3

6.7

247.46

142.69

9.8

48.0

0.94

23

chicken

24.5

14.1

141.7

124.7

20.9

30.4

3.67

24

swine

20.0

15.5

29.8

19.3

57.3

72.5

1.71

25

thermo-alkaline
thermo-acidic
thermo-acidic
ultrasonication
anaerobic
digestion
anaerobic
digestion
a

TS, total solids; VS, volatile solids; TKN, total Kjeldahl nitrogen; TON, total organic nitrogen; TAN, total ammonia nitrogen. bThe data presented
in the table were calculated according to the information provided in the related references.
F

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX

Research Article

ACS Sustainable Chemistry & Engineering

mental impacts associated with NOx and greenhouse gas

emissions.
The hybrid procedure of HTT followed by solid-state
ammonia stripping exhibits good performance in organic-N
decomposition and N recovery from CM as valuable ammonia
products, achieving not only an overall TN recovery eciency
of 57% but also the alleviation of environmental pollutions
associated with increasing input of active N. As for further
implementation of eective ammonia production and recovery
from manure wastes, investigations are underway so as to
accelerate ammonia production from the HTT process and
improve ammonia-N removal and recovery from the processed
manure.

mentioned above were detected to be 95.6%, 96.2%, 95.4%, and

96.6%, respectively, in agreement with the ammonia stripping
eciency when this system was applied to dry anaerobic
digested swine manure.17
Quantication of ammonia-N in HCl solutions demonstrates
that more than 96% of the removed ammonia-N from CM can
be eciently entrapped in the circulating system. After 3 h of
stripping, no signicant increase of SOC was observed in all of
the scrubbing solutions (p = 0.0613 > 0.05). Except for a trace
amount of acetic acid, neither carbohydrates nor proteins were
detected. Ammonia stripping at high TS content avoided the
foaming problems, preventing the contamination of acid
solutions from organic substances. In addition, the obtained
NH4Cl solutions can be used for fertilizer production or serve
other industrial purposes.
Methane Fermentation Trials by Using the AmmoniaStripped HTT Processed CM. The CH4 production
potentials of RCM and ammonia-stripped CM residues
(HTT180-15, HTT180-30, HTT180-60, and HTT220-0)
were assessed via 45 days of AD trials. The initial AD
conditions are listed in Table S3 (Supporting Information).
Results (Figure S2, Supporting Information) show that after
CM was processed at 180 C for 15, 30, and 60 min, CH4
evolution started earlier, and CH4 yields were recorded,
respectively, at 186.18, 195.53, and 158.55 mL/g-CMVS after
45 days of AD in comparison to 157.17 mL/g-CMVS from
RCM (without HTT and ammonia stripping). After 45 days of
AD, the concentration of ammonia-N in the RCM reactor was
1290.02 mg/L, whereas lower ammonia-N concentrations of
722.11, 708.23, 714.54, and 710.75 mg/L were detected in the
AD reactors of HTT180-15, HTT180-30, HTT180-60, and
HTT220-0, respectively. In addition to the immediate
availability of fermentable and soluble organic substances,
much lower levels of ammonia-N in the pretreated CM residues
might be attributable to their high CH4 yields. Therefore, the
enhancement eect is expected to be greater when AD for CH4
production is conducted under dry conditions after CM
samples were HTT processed and ammonia-stripped.
However, a remarkably low CH4 yield of 21.82 mL/g-CMVS
was obtained from HTT220-0 during the same period when
CM was pretreated at 220 C for 0 min and ammonia-stripped.
Ammonia toxicity was unlikely to be the reason for digestion
failure in this reactor since similar ammonia-N concentrations
were detected in the four digesters loaded with HTT processed
CM samples. Instead, the formation of some inhibitory or
nondegradable compounds (like melanoidins) during HTT at
this temperature might be accountable.9 Adaptation of
methanogens to these inhibitory substances might be necessary
if being used for CH4 production.
Environmental Implications. The large amount of CM
generated each year globally represents a source of N pollution
that requires proper disposal. Traditional practice of AD
followed by spreading of the digestate onto farmland has some
shortcomings such as low CH4 yield and insucient breakdown
of the organic manure, mainly due to ammonia toxicity and
high transportation cost when there is not enough arable land
nearby, and diculties in retention of N nutrient during storage
and spreading. In addition, high level of volatile ammonia in the
biogas is a problem of concern.26 Therefore, eective N
removal and recovery from the manure wastes prior to CH4
fermentation is crucial for controlling ammonia inhibition,
promoting CH4-based C capture and mitigating the environ-

ASSOCIATED CONTENT

S Supporting Information
*

The Supporting Information is available free of charge on the

ACS Publications website at DOI: 10.1021/acssuschemeng.6b00315.
Calculation of dry matter loss and nitrogen recovery
eciency through the HTT process; correlation
coecient matrix between two tested parameters in the
processed CM; initial CH4 fermentation conditions;
owchart of analytical procedures; variations of temperature in the HTT reactor under dierent operational
conditions; and cumulative CH4 production from nontreated RCM or the HTT processed and ammoniastripped CM samples (PDF)

AUTHOR INFORMATION

Corresponding Authors

*(Z.Z.) Tel/Fax: +81 298 534712. E-mail: zhang.zhenya.fu@u.

tsukuba.ac.jp.
*(Z.L.) Tel/Fax: +81 298 5346703. E-mail: lei.zhongfang.gu@
u.tsukuba.ac.jp.
Author Contributions

W.H. and T.Y. contributed equally to this work.

Notes

The authors declare no competing nancial interest.

ACKNOWLEDGMENTS
This work was supported by JSPS KAKENHI Grant Numbers
25281046, 15K00599, and 15K12235.
REFERENCES

(1) Miura, D.; Tezuka, T. A comparative study of ammonia energy

systems as a future energy carrier, with particular reference to vehicle
use in Japan. Energy 2014, 68, 428436.
(2) Vitousek, P. M.; Aber, J. D.; Howarth, R. W.; Likens, G. E.;
Matson, P. A.; Schindler, D. W.; Schlesinger, W. H.; Tilman, D.
Human alteration of the global nitrogen cycle: sources and
consequences. Ecol. Appl. 1997, 7, 737750.
(3) Lin, R.; Cheng, J.; Ding, L.; Song, W.; Qi, F.; Zhou, J.; Cen, K.
Subcritical water hydrolysis of rice straw for reducing sugar production
with focus on degradation by-products and kinetic analysis. Bioresour.
Technol. 2015, 186, 814.
(4) Yin, J.; Wang, K.; Yang, Y.; Shen, D.; Wang, M.; Mo, H.
Improving production of volatile fatty acids from food waste
fermentation by hydrothermal pretreatment. Bioresour. Technol.
2014, 171, 323329.
(5) Heilmann, S. M.; Molde, J. S.; Timler, J. G.; Wood, B. M.;
Mikula, A. L.; Vozhdayev, G. V.; Colosky, E. C.; Spokas, K. A.;
Valentas, K. J. Phosphorus Reclamation through Hydrothermal

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX

Research Article

ACS Sustainable Chemistry & Engineering

Carbonization of Animal Manures. Environ. Sci. Technol. 2014, 48,
1032310329.
(6) Qian, T.-T.; Jiang, H. Migration of Phosphorus in Sewage Sludge
during Different Thermal Treatment Processes. ACS Sustainable Chem.
Eng. 2014, 2, 14111419.
(7) Berge, N. D.; Ro, K. S.; Mao, J.; Flora, J. R. V.; Chappell, M. A.;
Bae, S. Hydrothermal carbonization of municipal waste streams.
Environ. Sci. Technol. 2011, 45, 56965703.
(8) Yu, G.; Zhang, Y.; Schideman, L.; Funk, T.; Wang, Z.
Distributions of carbon and nitrogen in the products from hydrothermal liquefaction of low-lipid microalgae. Energy Environ. Sci. 2011,
4, 45874595.
(9) Bougrier, C.; Delgenes, J. P.; Carrere, H. Effects of thermal
treatments on five different waste activated sludge samples
solubilisation, physical properties and anaerobic digestion. Chem.
Eng. J. 2008, 139, 236244.
(10) Carrere, H.; Sialve, B.; Bernet, N. Improving pig manure
conversion into biogas by thermal and thermo-chemical pretreatments.
Bioresour. Technol. 2009, 100, 36903694.
(11) He, C.; Wang, K.; Yang, Y.; Amaniampong, P. N.; Wang, J. Y.
Effective nitrogen removal and recovery from dewatered sewage sludge
using a novel integrated system of accelerated hydrothermal
deamination and air stripping. Environ. Sci. Technol. 2015, 49, 6872
6880.
(12) Oliviero, L.; Barbier, J.; Duprez, D., Jr. Wet Air Oxidation of
nitrogen-containing organic compounds and ammonia in aqueous
media. Appl. Catal., B 2003, 40, 163184.
(13) Oulego, P.; Laca, A.; Diaz, M. Kinetics and Pathways of Cyanide
Degradation at High Temperatures and Pressures. Environ. Sci.
Technol. 2013, 47, 15421549.
(14) Sato, N.; Quitain, A. T.; Kang, K.; Daimon, H.; Fujie, K.
Reaction kinetics of amino acid decomposition in high-temperature
and high-pressure water. Ind. Eng. Chem. Res. 2004, 43, 32173222.
(15) Wilson, C. A.; Novak, J. T. Hydrolysis of macromolecular
components of primary and secondary wastewater sludge by thermal
hydrolytic pretreatment. Water Res. 2009, 43, 44894498.
(16) Dwyer, J.; Starrenburg, D.; Tait, S.; Barr, K.; Batstone, D. J.;
Lant, P. Decreasing activated sludge thermal hydrolysis temperature
reduces product colour, without decreasing degradability. Water Res.
2008, 42, 46994709.
(17) Huang, W.; Huang, W.; Yuan, T.; Zhao, Z.; Cai, W.; Zhang, Z.;
Lei, Z.; Feng, C. Volatile fatty acids (VFAs) production from swine
manure through short-term dry anaerobic digestion and its separation
from nitrogen and phosphorus resources in the digestate. Water Res.
2016, 90, 344353.
(18) APHA (American Public Health Association). Standard Methods
for the Examination of Water and Wastewater; American Public Health
Association/American Water Work Association/Water Environment
Federation: Washington, D.C., 2012.
(19) Herbert, D.; Phillips, P. J.; Strange, R. E. Chemical Analysis of
Microbial Cells. In Methods in Microbiology; Norris, J. R., Ribbons, D.
W., Eds.; Academic Press: London, U.K., 1971; Vol. 58, pp 265277.
(20) Bradford, M. M. A rapid and sensitive method for the
quantitation of microgram quantities of protein utilizing the principle
of protein-dye binding. Anal. Biochem. 1976, 72, 248254.
(21) Donoso-Bravo, A.; Perez-Elvira, S.; Aymerich, E.; Fdz-Polanco,
F. Assessment of the influence of thermal pre-treatment time on the
macromolecular composition and anaerobic biodegradability of sewage
sludge. Bioresour. Technol. 2011, 102, 660666.
(22) Jin, Y.; Hu, Z.; Wen, Z. Enhancing anaerobic digestibility and
phosphorus recovery of dairy manure through microwave-based
thermochemical pretreatment. Water Res. 2009, 43, 34933502.
(23) Elbeshbishy, E.; Aldin, S.; Hafez, H.; Nakhla, G.; Ray, M. Impact
of ultrasonication of hog manure on anaerobic digestability. Ultrason.
Sonochem. 2011, 18, 164171.
(24) Abouelenien, F.; Kitamura, Y.; Nishio, N.; Nakashimada, Y. Dry
anaerobic ammonia-methane production from chicken manure. Appl.
Microbiol. Biotechnol. 2009, 82, 757764.

(25) Huang, W.; Zhao, Z.; Yuan, T.; Lei, Z.; Cai, W.; Li, H.; Zhang,
Z. Effective ammonia recovery from swine excreta through dry
anaerobic digestion followed by ammonia stripping at high total solids
content. Biomass Bioenergy 2016, 90, 139147.
(26) Appels, L.; Baeyens, J.; Degreve, J.; Dewil, R. Principles and
potential of the anaerobic digestion of waste-activated sludge. Prog.
Energy Combust. Sci. 2008, 34, 755781.

DOI: 10.1021/acssuschemeng.6b00315
ACS Sustainable Chem. Eng. XXXX, XXX, XXXXXX