From sewage sludge ash to a recycled feed phosphate - digestibility of precipitated calcium phosphate in broiler chickens and growing pigs

Abstract

Today, EU is largely (∼92%) dependent on the import of phosphates as most mines are located outside Europe. Because of the limited availability, phosphorus (P) is included on the list of Critical Raw Materials. Precipitated calcium phosphate (PCP) recovered from sewage sludge ash is a novel and sustainable option to replace mined P as raw material in feed phosphates, e.g. monocalcium phosphate (MCP) or dicalcium phosphate, but the digestibility has not yet been tested in vivo. The aim was therefore to determine PCP and MCP apparent ileal digestibility (AID) of P in broiler chickens and apparent (ATTD) and true (TTTD) total tract digestibility of P in growing pigs. A chicken study comprised 240 Ross 308 chickens that were housed in groups of eight from day 21 to day 28. Five diets were used, a basal diet and two test diets, which contributed either 0.075% (low) or 0.150% (high) additional P for each of the test sources (MCP and PCP). The basal and test diets were composed to achieve increasing levels of P and AID was calculated with regression analysis. In the pig study, eight individually housed pigs were used in a change-over study with two experimental periods. The pigs were fed a basal P-free diet in a preperiod to be able to estimate endogenous P losses and then two different diets in two periods using a change-over design, where MCP and PCP were the only P source, providing in total 0.33 (basal diet), 4.42 (MCP) and 3.53 (PCP) g kg-1P, respectively. The AID of P in PCP and MCP for chickens was 58.4 and 75.1% (P = 0.166). The ATTD and TTTD of P in PCP for pigs were 58.4 and 67.2%, respectively, which was lower (P

Full text

From sewage sludge ash to a recycled feed phosphate – digestibility of
precipitated calcium phosphate in broiler chickens and growing pigs
M. Presto Åkerfeldt
a,
⇑
, S. Stiernström
b
, K. Sigfridson
c
, E. Ivarsson
a
a
Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, Box 7024, 75007 Uppsala, Sweden
b
EasyMining Services Sweden AB, Ultunaallén 2A, 756 51 Uppsala, Sweden
c
Lantmännen Lantbruk, 205 03 Malmö, Sweden
article info
Article history:
Received 7 November 2022
Revised 4 April 2023
Accepted 6 April 2023
Available online 17 April 2023
Keywords:
Digestible P
Environment
Feed formulation
Monogastric animals
Recovered P
abstract
Today, EU is largely (92%) dependent on the import of phosphates as most mines are located outside
Europe. Because of the limited availability, phosphorus (P) is included on the list of Critical Raw
Materials. Precipitated calcium phosphate (PCP) recovered from sewage sludge ash is a novel and sus-
tainable option to replace mined P as raw material in feed phosphates, e.g. monocalcium phosphate
(MCP) or dicalcium phosphate, but the digestibility has not yet been tested in vivo. The aim was therefore
to determine PCP and MCP apparent ileal digestibility (AID) of P in broiler chickens and apparent (ATTD)
and true (TTTD) total tract digestibility of P in growing pigs. A chicken study comprised 240 Ross 308
chickens that were housed in groups of eight from day 21 to day 28. Five diets were used, a basal diet
and two test diets, which contributed either 0.075% (low) or 0.150% (high) additional P for each of the
test sources (MCP and PCP). The basal and test diets were composed to achieve increasing levels of P
and AID was calculated with regression analysis. In the pig study, eight individually housed pigs were
used in a change-over study with two experimental periods. The pigs were fed a basal P-free diet in a
preperiod to be able to estimate endogenous P losses and then two different diets in two periods using
a change-over design, where MCP and PCP were the only P source, providing in total 0.33 (basal diet),
4.42 (MCP) and 3.53 (PCP) g kg
-1
P, respectively. The AID of P in PCP and MCP for chickens was 58.4
and 75.1% (P= 0.166). The ATTD and TTTD of P in PCP for pigs were 58.4 and 67.2%, respectively, which
was lower (P< 0.001) than the corresponding values for MCP (82.1 and 89.1%), respectively. The
digestibility of calcium (Ca) did not differ in the chicken diets with high inclusion levels of PCP and
MCP (54.7 and 55.3%, respectively, P= 0.535), but was lower for PCP than MCP in the pig study (57.8
and 70.8% respectively, P= 0.001). In conclusion, the digestibility of P in PCP for chickens did not differ
from conventional MCP, whereas for pigs, it was lower, but could be a viable alternative to other common
sources of P.
Ó2023 The Authors. Published by Elsevier B.V. on behalf of The Animal Consortium. Thisis anopenaccess
article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Implications
The transition to circular economy is crucial in building a sus-
tainable society. In this context, phosphorus is a key factor. Today,
the EU is largely dependent on import as most mines are located
outside Europe. The large ecological footprint from mining and long
transports makes safe recycling of phosphorus substantial to
strengthen the EU food value chain. Precipitated calcium phosphate
recovered from sewage sludge ash has the potential to be used as an
alternative feed phosphate, and this study provides in vivo
digestibility of phosphorus and calcium of this alternative feed
phosphate in poultry and pigs. Recycled phosphorus in animal feed
aligns with EU’s green deal and farm-to-fork strategy, securing
domestic supply and saving significant amounts of CO
2
emissions.
Introduction
The transition to a circular economy is crucial in building a sus-
tainable society. Today, almost half of our climate impact and 90%
of water scarcity issues are linked to the way we extract resources
and produce goods and food (IRP, 2019). In this context, phospho-
rus (P) has a key function. Clearly, fertilisers are vital for global
food production (Ritchie, 2021). In addition, the geopolitical
instability leads to problems with sourcing fertilisers and P to
make fertilisers. The EU’s fertiliser and animal food industries, as
well as other industry sectors using P compounds, are highly reli-
ant on imports of phosphate rock with a large ecological footprint.
https://doi.org/10.1016/j.animal.2023.100819
1751-7311/Ó2023 The Authors. Published by Elsevier B.V. on behalf of The Animal Consortium.
This is an open accessarticle under the CCBY license (http://creativecommons.org/licenses/by/4.0/).
⇑
Corresponding author.
E-mail address: magdalena.akerfeldt@slu.se (M. Presto Åkerfeldt).
Animal 17 (2023) 100819
Contents lists available at ScienceDirect
Animal
The international journal of animal biosciences

Today, EU is largely (92%) dependent on import as most mines are
located outside Europe, mainly in Morocco and Russia (Brownlie
et al., 2022). P is non-substitutable in fertilisers and feed and,
therefore, is included on EU’s list of Critical Raw Materials (EC,
2020) and with increased demand for resource efficiency and more
sustainable value chains, the use of recycled P will be unavoidable
in the future society. P can be recovered from sewage sludge by
precipitation, which has shown high bioavailability of P for plants
(Shiba and Ntuli, 2017).
Within pig and poultry production, P is added in the feed. The
amount of the added P that animals can utilise differs between dif-
ferent feedstuffs (Jongbloed and Kemme, 1990). The P that is not
digested by the animal is excreted in faeces and urine and con-
tributes to the leakage of nutrients and the environmental burden.
To avoid this, the correct amount of P with a high digestibility
should be added to the feed. In feed formulation, this requires that
the digestibility of the feed ingredients is known. EasyMining, a
Swedish innovation company, Uppsala, Sweden, dedicated to clos-
ing nutrient cycles, has invented a process that recovers P from
sewage sludge ash (EasyMining, 2022) to produce a precipitated
calcium phosphate (PCP). The PCP is a pure product that fulfils
quality demands in feed legislation (EU, 2002, 2003, and 2006)
(Table 1). The main benefit with using recycled calcium phosphate
such as PCP is closing of the P cycle, resulting in reduced need for
rock phosphate and imports from outside Europe by having
domestic production of phosphates with decreasing CO
2
emissions
(Johansson, 2020). The PCP have a potential to be used as a feed
ingredient, but to be so, the P digestibility in monogastric animals
such as chickens and pigs need to be determined and tested in vivo.
The aim of this project was therefore to determine the P
digestibility of PCP in growing chickens and pigs. The hypothesis
was that PCP should have a comparable P digestibility for both
chickens and pigs as conventional monocalcium phosphate
(MCP) and dicalcium phosphate (DCP).
Material and methods
Test sources monocalcium phosphate and precipitated calcium
phosphate
The P source in MCP used was a commercial (MCP BOLIFOR
Ò
,
MCP-F, YARA). P in PCP was efficiently recovered from incinerated
sewage sludge according to the Ash2
Ò
Phos-process. The process
consisted of three steps that allow to separate elements of interest
and detoxify the products; a first acidic step, a second alkaline step
(where intermediate products are produced), and a final conver-
sion step where the intermediates are processed into final prod-
ucts. The main inputs of the process were ash from incinerated
sewage sludge, acid (hydrochloric acid) and lime (EasyMining,
2022). The PCP fulfilled the quality demands in the feed legislation
with lower values than the legal limits for fluorine, cadmium,
arsenic, mercury, lead, dioxins and polychlorinated biphenyl (EU,
2002, 2003, and 2006)(Table 1). Limit values for aluminium and
nickel are not listed in the EU legislation on undesirable substances
in animal feed, but levels for toxicity can be found for the total
intake of feed. The dietary inclusion level of PCP was 0.45, 0.91
and 2.23% in the chicken (Table 2) and pig (Table 3) diets, and
the values of aluminium and nickel in the diets corresponded to
7.7, 15.5 and 37.9 mg kg
1
and were below toxicity for chickens
and pigs according to NRC (2005) and EFSA (2015). The solubility
of P in 2% citric acid was tested in both MCP and PCP according
to the procedure described by IFP (2023). The solubility test was
done in duplicates and average dissolution degrees were calculated
and the result for PCP and MCP is shown in Table 1.
Experimental design and housing – chicken study
The chicken study was performed at the Swedish Livestock
Research Centre, SLU, Uppsala. A total of 240 one-day-old chicks
(Ross 308) was divided into 30 groups with eight chickens/group.
The chickens were housed in pens raised from the floor with solid
floor covered by wood shavings, with free access to feed and water
throughout the experiment. From days 1–21, the chickens were fed
a commercial poultry feed based on wheat and soybean meal
(Johan Hansson AB, Sweden), all feed were free from coccidostats.
On day 21, the actual digestibility study started. The digestibility
study included five experimental diets, a basal diet composed to
fulfil the protocol requirements stated in WPSA (2013;Table 2).
In addition, two experimental diets were used to determine the P
digestibility of the test sources, PCP and MCP (Bolifor MCP-F, Yara,
Sweden). These were supplemented at two levels; 0.075 (low) and
0.15% (high), in order to achieve an increase in the total P level in
the diet compared to the basal diet (Table 2) and perform regres-
sion analysis with the slope being the digestible coefficient. Tita-
nium dioxide (TiO
2
)was added with 5 g kg
1
to all diets as an
indigestible marker. The Ca:P ratio was optimised to be maintained
at 1.3 for all diets, and other nutrients such as vitamins, minerals
and trace elements were optimised to be provided in adequate
amounts and to not differ between the experimental diets. All
ingredients were milled through a hammer mill with a 3-mm
screen before mixed and steam pelleted (conditioning temperature
75 °C) through a 3-mm die; the temperature of the feed after pel-
leting was 83.6 °C.
The chickens were weighed weekly, and dietary treatments
were distributed to get similar starting weight for all treatments.
The average weight of the chickens on day 21 was 1016.2 g ± 186 g,
and there was no difference (P= 0.998) in start weight between the
treatments. The chickens were fed the experimental diets between
day 21 and day 28, the amount of feed given and feed residues as
well as BW were registered on pen basis weekly. Between days
0 and 21, the feed intake was 1351.3 ± 70.61 g/chicken and the feed
conversion ratio was 1.39 ± 0.086. On day 28, the chickens were
killed by an intravenous injection of sodium pentobarbital through
the wing vein. The digestive tract was removed, and the gut con-
tent from ileum identified as the part from Meckel’s Diverticulum
to the ileo-caecal-colonic junction was collected. Samples from
birds in the same pen were pooled and stored at 20 °C and
freeze-dried before analysis.
Table 1
Analysed solubility in 2% citric acid, mineral, trace mineral and content of dioxins and
polychlorinated biphenyl in MCP and PCP used in the pig and chicken feed.
Item MCP
1
PCP
Chemical formula Ca(H
2
PO
4
)
2
H
2
OCa
5
(PO
4
)
3
OH
Solubility in 2% citric acid, % 86 87
Ca, g/kg 165 350
P, g/kg 249 175
Mg, g/kg 10 4.1
F, g/kg 2 14
Fe, g/kg . 1.4
Al, g/kg . 1.7
As, mg/kg <10 1.4
Cd, mg/kg <10 <0.1
Pb, mg/kg <15 3.6
Hg, mg/kg <0.1 <0.1
Cu, mg/kg . 5
Cr, mg/kg . 1.7
Co, mg/kg . 0.7
Ni, mg/kg . 2.5
Dioxins, mg/kg . <0.1
Polychlorinated biphenyl, mg/kg . <0.1
Abbreviations: MCP = monocalcium phosphate, PCP = precipitated calcium
phosphate.
1
BOLIFOR
Ò
, MCP-F, YARA, Pocklington York, UK. Indicates that data are not
available.
M. Presto Åkerfeldt, S. Stiernström, K. Sigfridson et al. Animal 17 (2023) 100819
2

Experimental design and housing – pig study
The study was performed at the Centre of Veterinary Medicine
and Animal Science at the Swedish University of Agricultural
Sciences, Uppsala in May and June 2021. Eight pigs
(Yorkshire Hampshire) were used in the study and were 9 weeks
old at the start of the experiment with and average weight of 24.
9 ± 3.19 kg. All pigs were gilts from two litters, and the experimen-
tal diets were randomly distributed within litter. The pigs were fed
a basal P-free diet (0.33 g/kg
1
DM) in a preperiod (fed prior to the
test diets) to be able to estimate endogenous P losses (ELP). Two
test diets with different test sources of phosphorus, PCP and
MCP, with similar P and Ca levels, were then fed to the pigs in
two periods using a change-over design. The MCP and PCP diets
provided in total of 4.42 and 3.53 g kg
1
DM of P and 7.51 and
7.35 g kg
1
DM of Ca, respectively. TiO
2
was added with
2.5 g kg
1
to all diets as an indigestible marker. All diets are shown
in Table 3. The pigs were kept in individual pens with nose contact
with the neighbouring pig. They did not have access to straw, but
the pens were equipped with a rubber mat, and the pigs had access
to plastic and rubber toys to enable explorative behaviour. The
basal-diet and the experimental diets were fed to the pigs during
11 days in each period (preperiod, period 1 and period 2), consist-
ing of 7 days of adjustment to the diet, followed by 4 days of faeces
collection. The feed allowance was 4% of the pig BW, divided into
two equal meals. The diets were meal feed and water was added
and mixed with the feed prior to each feeding in a ratio of 2:1. Fae-
ces were collected after the pigs had defecated, from carefully
cleaned floors. A pooled sample from the four days of faecal sam-
pling was used for analysis. The samples were stored in freezer
20 °C and were freeze-dried before analysis.
Chemical analyses and calculations
The digesta and faeces were freeze-dried before analysis. Feed
and digesta were analysed for DM, CP, TiO
2
, Ca and P. The feed, ileal
digesta and faecal samples were analysed for DM by drying at
103 °C for 16 h and for ash after ignition at 550 °C for 3 h. TiO
2
in feed ileal digesta and faecal samples was analysed according
to Short et al. (1996) on 0.1 g samples of ileal and faecal samples
and 0.5 g of feed samples and was used as an indigestible marker
for calculations of AID and ATTD coefficients. Ca and P were anal-
ysed according to Swedish standard (Svensk Standard SS 02 83
11) with some minor modifications. Briefly, 1 g sample was
weighed in and 20 mL 7 M HNO
3
was added and boiled for 1 h with
mixing after 15 and 45 min. The samples were cooled, and deio-
nised water was added to reach a total volume of 100 mL before
mixing. The samples were thereafter diluted, mixed and cen-
trifuged, and the Ca and P level was measured with a Spectro Blue
ICP Spectrometer, Spectro Ametek, Kleve, Germany.
The ileal apparent digestibility (IAD) and apparent total tract
digestibility (ATTD) for the diets were calculated using the indica-
tor technique (Sauer et al. 2000) according to the equation:
IAD=ATTD ð%Þ¼100 ½100 ðTiO
2D
PC
Dig=F
Þ=ðTiO
2Dig=F
PC
D
Þ
where TiO
2D
is the TiO
2
concentration in diet (g kg
1
DM), PC
Dig/F
is
the P concentration (g kg
1
DM) in digesta/faeces, TiO
2Dig/F
is the
TiO
2
concentration (g kg
1
DM) in digesta/faeces and PC
D
is the P
concentration (g kg
1
DM) in diet.
The content of precaecal digestible P (pcdP) in the chicken diet
was calculated according to WPSA (2013) as:
pcdP ðgkg
1
DMÞ¼IAD ð%ÞPC
D
=100
Table 2
Ingredient composition of experimental diets used to determine P digestibility of monocalcium phosphate (MCP) and precipitated calcium phosphate (PCP) when supplemented
at two levels in chickens, and its optimised and analysed chemical composition.
Item Basal MCP Low MCP High PCP Low PCP High
Ingredients, %
Corn 40.00 40.00 40.00 40.00 40.00
Wheat 23.31 23.33 23.35 23.61 23.32
Soybean meal 15.00 15.00 15.00 15.00 15.00
Wheat starch 10.85 10.07 9.29 10.06 9.82
Potato protein 7.45 7.45 7.46 7.41 7.46
Soybean Oil 0.62 0.94 1.25 0.86 1.04
Limestone 0.79 0.90 1.01 0.64 0.47
Titanium dioxide 0.50 0.50 0.50 0.50 0.50
PCP 0 0 0 0.45 0.91
MCP 0 0.33 0.66 0 0
Premix
1
0.51 0.51 0.51 0.51 0.51
Sodium bicarbonate 0.24 0.24 0.24 0.24 0.24
Methionine 0.22 0.22 0.22 0.22 0.22
NaCl 0.20 0.20 0.20 0.20 0.20
Choline Chloride 0.12 0.12 0.12 0.12 0.12
L-Lysine 0.12 0.12 0.12 0.12 0.12
L-Arginine 0.09 0.09 0.09 0.09 0.09
Optimised chemical composition
DM 873.6 874.5 875.3 874.2 874.7
Calcium, g kg
1
DM 4.61 5.72 6.83 5.72 6.84
Phosphorus, g kg
1
DM 3.55 4.40 5.26 4.40 5.26
Ca/P 1.30 1.30 1.30 1.30 1.30
Analysed chemical composition
DM 912.8 914.8 911.3 913.9 915.4
Ash, g kg
1
DM 43.80 48.30 46.10 48.20 45.30
Calcium, g kg
1
DM 5.35 6.28 7.33 6.14 7.19
Phosphorus, g kg
1
DM 3.89 4.25 5.05 4.20 4.89
Ca/P 1.38 1.48 1.45 1.46 1.47
1
The premix provided (per kg feed): Vitamin A (retinyl acetate): 9 900 IE; Vitamin D3 (cholecalciferol) 2 475 IE; Vitamin E (alpha-tocopheryl acetate): 64.4 mg; Vitamin B1
(thiamine mononitrate): 2.0 mg; Vitamin B2: 6.0 mg; Niacin: 30 mg; Vitamin B5 (calcium-D-pantothenate): 15 mg; Vitamin B6 (pyridoxine hydrochloride): 6 mg; Biotin:
0.2 mg; Vitamin B9 (folic acid): 1.6 mg; Vitamin B12 (cyanocobalamin): 0.02 mg; Vitamin K3 (menadione nicotinamide bisulphite): 3.09 mg; Fe (iron sulphate): 52.5; Zn (zinc
sulphate):82.5 mg; Cu (copper sulphate):15 mg; I (calcium iodate): 1.05; Mn (manganese sulphate): 127.5 mg; Se (sodium celite): 0.3 mg.
M. Presto Åkerfeldt, S. Stiernström, K. Sigfridson et al. Animal 17 (2023) 100819
3

where IAD is the ileal apparent digestibility for the diet and PC
D
is
the P concentration (g kg
1
DM) in diet.
The ELP that is referred to the basal diet free of P was estimated
as described by Mariscal-Landín and Reis de Souza (2006) accord-
ing to the following equation:
ELP ðgkg
1
DMIÞ¼ðPC
F
ðTiO
2B
=TiO
2F
ÞÞDMI
B
where PC
F
is the P concentration in faeces (g kg
1
DM), TiO
2B
is the
TiO
2
concentration in the basal diet (g kg
1
DM), TiO
2F
is the TiO
2
concentration in faeces (g kg
1
DM) and DMI
B
is the DM intake of
the basal diet (kg day
1
).
To calculate the true total tract digestibility (TTTD) of P, the
equation by Furuya and Kaji (1991) was used:
TTTD ð%Þ¼ATTD þðELP=PC
D
Þ100
where ATTD is the apparent total tract digestibility of P (%) in the
diet, ELP is the endogenous losses of P (g kg
1
DMI) and PC
D
is
the P concentration (g kg
1
DM) in the diet.
Statistical analyses
In the chicken study, one value was classified as an outlier since
the IAD of P was two SD from the treatment mean, and excluded
from the statistical analysis. In the pig study, one pig was excluded
from the statistical analysis due to values that were classified as
outliers since the ATTD of Ca and TTTD of P was two SD from the
treatment mean. The statistical analysis was performed with the
Mixed procedure in SAS
Ò
9.4 (SAS Institute Inc., 2021) to determine
treatment effects by ANOVA. For the chicken study, the model
included diet as a fixed factor, and pen as a random factor. Pen
served as experimental unit. In the pig study, diet and period were
used as fixed factors and pig as random factor. P-values <0.05 were
considered significant. To estimate the digestibility of PCP and MCP
in the chicken study, a multiple regression analysis with a common
intercept was performed in the GLM procedure between the total P
contents and the pcdP in the diets, where the slope is the
digestibility of the P source.
Results
Chicken study
The BW on day 28 was 1701.3 ± 135.58 g (mean ± SD), the feed
intake between day 21 - day 28 was 895.6 ± 102.38 (mean ± SD)
and feed conversion ratio between days 21 and day 28 was
1.34 ± 0.088 (mean ± SD). None of these parameters differed
between the diets. The IAD of organic matter and Ca did not differ
between diets, whereas the IAD of P was higher in the MCP high
diet than in the other diets (P= 0.022) and pcdP were higher in
both PCP and MCP high diets compared with PCP and MCP low
(P= 0.001) (Table 4). The linear relationship between the total P
content in the diet and pcdP is shown in Table 5. The IAD of P in
MCP was estimated to 75.1% and in PCP to 58.4% (P= 0.166). The
amount of P in MCP and PCP was 227 and 165 g kg
1
; thus, the
amount of digestible P was 170.5 g kg
1
for MCP and 96.4 g kg
1
for PCP.
Pig study
For pig start and final weights as well as growth rate, there were
no effects of diet. Although, as expected, an effect of period was
found and the final weight was 30.1 ± 4.97 and 35.6 ± 1.27 kg
(mean ± SD) for period I and period II, respectively. The ATTD of
organic matter did not differ between the MCP and PCP diets, but
a diet effect was found for the ATTD of Ca and P with higher
digestibility of both Ca and P for MCP compared with PCP
(P= 0.001). The estimated ELP ranged between 270 and 363 (aver-
age 309) mg kg
1
DMI, and the TTTD of P corrected for endogenous
losses were correspondingly higher than the values for ATTD of P
(Table 6) but showed a diet effect with higher TTTD for MCP com-
pared with PCP (P= 0.001). Period had no effect on either ATTD or
TTTD of OM, Ca or P. The amount of P in MCP and PCP was 227 and
165 g kg
1
. Using the ATTD, the amount of digestible P was
186.4 g kg
1
for MCP and 96.4 g kg
1
for PCP. The corresponding
digestible P based on the TTTD were 202.3 g kg
1
for MCP and
110.9 g kg
1
for PCP.
Discussion
The PCP recovered from incinerated sewage sludge demonstrate
a pure product showing lower levels than the legal limits for fluo-
rine, cadmium, arsenic, mercury, lead, dioxins and polychlorinated
biphenyl. The level of aluminium and nickel in the diets was also
below-recommended toxicity levels for chicken and pigs (NRC,
2005; EFSA, 2015). In both the chicken and pig study, the growth
performance was within the expected range and did not differ
between diets. The feed intake and growth rate of the chickens
were within 10% deviation from expected growth performance of
Table 3
Ingredient composition of a basal diet to determine endogenous P losses (ELP) and
two experimental diets used to determine the P digestibility of monocalcium
phosphate (MCP) and precipitated calcium phosphate (PCP) in the pig study, and its
optimised and analysed chemical composition in g kg
1
DM.
Item Basal MCP PCP
Ingredient (%)
Corn starch 50.87 49.99 50.56
Dextrose 18.00 18.00 18.00
Potatao protein 18.00 18.00 18.00
Rape seed oil 5.00 5.00 5.00
Cellulose 4.00 4.00 4.00
Limestone 1.92 1.18 0
MCP 0 1.62 0
PCP 0 0 2.23
Sodium bicarbonate 0.40 0.40 0.40
NaCl 0.39 0.39 0.39
Lysine-HCl 0.35 0.35 0.35
Premix 0.320 0.320 0.320
Methionine-DL 0.27 0.27 0.27
Titanium dioxide 0.25 0.25 0.25
Magnesium oxide 0.10 0.10 0.10
Threonine 0.05 0.05 0.05
Tryptophan 0.057 0.057 0.057
Zinc sulphate 0.021 0.021 0.021
Sodium selenite 0.001 0.001 0.001
Optimised chemical composition
1
DM 916.5 917.3 916.5
Calcium, g kg
1
DM 7.84 7.84 8.81
Phosphorus, g kg
1
DM 0.59 4.60 4.60
Ca/P 13.3 1.70 1.92
Magnesium, g kg
1
DM 0.88 0.96 0.73
Potassium, g kg
1
DM 1.16 1.16 1.14
Chloride, g kg
1
DM 3.67 3.67 3.67
Sodium, g kg
1
DM 2.97 2.97 2.95
Iron, mg kg
1
DM 212.4 232.0 132.7
Copper, mg kg
1
DM 19.2 19.2 19.2
Manganese, mg kg
1
DM 52.1 46.9 24.5
Zinc, mg kg
1
DM 86.7 87.6 85.7
Analysed chemical composition
DM 934.0 929.3 930.8
Ash, g kg
1
DM 31.7 41.4 36.9
Calcium, g kg
1
DM 6.84 7.51 7.35
Phosphorus, g kg
1
DM 0.33 4.42 3.53
Ca/P 20.7 1.70 2.08
1
The diet provided (mg kg
1
): Pantothenic acid 12.24; Choline 45.0; Vitamin B3
Niacin 20.4; Vitamin E 61.2; Vitamin B1 2.04; Vitamin B12 0.02; Vitamin B2 4.08;
Vitamin B6 3.06 and (IE kg
1
): Vitamin D3 510; Vitamin A 5 100.
M. Presto Åkerfeldt, S. Stiernström, K. Sigfridson et al. Animal 17 (2023) 100819
4

Ross 308 (Aviagen, 2019), which is one of the criteria of the WPSA
(2013) protocol. A higher BW was observed for period I than period
II in the pig study and was expected, as the pigs were older in per-
iod II. Since the pigs were given a restricted amount of feed, the
pigs were not expected to reach their maximal genetic growth
potential and the results should therefore not be compared to
growth studies.
We hypothesised that PCP should have a similar P digestibility
as MCP for both chickens and pigs. The obtained results could how-
ever not fully support this and lower P digestibility of PCP than
MCP was found in pigs and although not significantly different,
numerically lower values were observed also in chickens. Accord-
ing to our knowledge, this is the first time the digestibility of PCP
is determined in vivo, whereas previous research has evaluated
the digestibility of other feed phosphates, e.g. MCP, DCP, monodi-
calcium phosphate, defluorinated phosphate, monosodium phos-
phate and tricalcium phosphate. According to previous results
(summarised in Table 7), the reported P digestibility of MCP in
the present studies is judged to be within expected range. The
tested PCP had lower digestibility compared to MCP in general,
but show similar P digestibility as DCP and monodicalcium phos-
phate for chickens.
By using a P-free basal diet, the P that is excreted by the animal
is of endogenous origin, and the basal endogenous losses of P can
be estimated (Petersen and Stein 2006). Correction for the basal
ELP from the ATTD allows for the determination of true total tract
digestibility (TTTD), which can be assumed as an accurate estima-
tion of the bioavailable P (Petersen et al. 2011; Baker et al. 2013). In
the present study, a P-free diet was used, which made it possible to
determine ELP and TTAD of the MCP and PCP. However, the ELP in
the present study were higher (average 309 mg kg
1
DM) than pre-
viously reported values of 210 and 139 mg kg
1
of DMI (Ajakaiye
et al. 2003; Petersen and Stein 2006). On the other hand, losses
of endogenous P have been ranging between 70 mg kg
1
of DMI
(Dilger and Adeola 2006; Pettey et al. 2006) and 670 mg kg
1
of
DMI (Shen et al. 2002). The higher values might be a result of using
different estimation procedures, such as the regression procedure
(Dilger and Adeola 2006) or that digestibility measurements are
used with different techniques, for example the use of and indi-
gestible marker or total faecal collection in metabolism cages. Also,
dietary factors in diets containing commonly used feed ingredients
Table 4
Ileal apparent digestibility (%) of organic matter, Ca and P as well as the pcdP (g kg
1
DM) of MCP and PCP when supplemented at two levels (low and high) in chickens.
Item Basal PCP Low MCP Low PCP High MCP High SEM P-value
Organic matter 73.43 73.73 74.41 75.76 75.60 0.770 0.150
Ca 59.03 55.13 58.13 54.71 55.34 2.196 0.535
P 41.91
ab
40.28
b
42.64
ab
44.16
ab
48.27
a
2.007 0.022
PcdP 1.61
b
1.67
b
1.79
b
2.16
a
2.43
a
0.094 0.001
Abbreviations: MCP = monocalcium phosphate, PCP = precipitated calcium phosphate, pcdP = precaecal digestible P.
a,b
Values within a row with different superscripts differ significantly at P< 0.05.
Table 5
Linear relationship between precaecal digestible P content (g kg
1
DM) and total P of monocalcium phosphate (MCP) and precipitated calcium phosphate (PCP) in chickens.
Item Regression equation SE of slope SE intercept R
2
Ileal digestibility, % P-value
Test source
MCP Y = 0.751X 0.638 0.142 0.620 0.770 75.1 0.166
PCP Y = 0.584X 0.603 0.110 0.475 0.770 58.4
Table 6
ATTD (%) of organic matter, Ca and P and TTTD (%) of MCP and PCP in pigs.
Item MCP PCP SEM P-value
ATTD of organic matter 94.2 94.0 0.24 0.348
ATTD of Ca 71.3 58.5 2.29 0.001
ATTD of P 82.1 58.4 2.02 0.001
TTTD of P 89.1 67.2 2.00 0.001
Abbreviations: MCP = monocalcium phosphate, PCP = precipitated calcium phos-
phate, ATTD = apparent total tract digestibility, TTTD = true total tract digestibility.
Table 7
Comparison between IAD, ATTD, STTD and TTTD (%) of P of different feed phosphates for chickens and pigs in the present study and previous research.
Item PCP MCP DCP MDCP DFP MSP TCP Reference
Chicken
IAD 78.3 59.0 70.7 31.5 Bikker et al. (2016)
64.6 69.3 60.2 Trairatapiwan et al. (2018)
58.4 75.1 Present study
Pig
ATTD 84.0
1
88.0
2
Lopez Diaz (2020)
83.0–88.0 81.0 Petersen and Stein (2006)
85.9 78.4 78.0 87.3 65.2 Kwon and Kim (2017)
58.4 82.1 – – – – – Present study
STTD – 93.0 87.0 86.5 - 94.9 71.3 Kwon and Kim (2017)
TTTD – 88.6–94.9
3
81.5 – – 98.2 – Petersen and Stein (2006)
67.2 89.1 Present study
Abbreviations: IAD = ileal apparent digestibility; ATTD = apparent total tract digestibility; STTD = standardised total tract digestibility; TTTD = true total tract digestibility;
PCP = precipitated calcium phosphate, MCP = monocalcium phosphate, DCP = dicalcium phosphate; MDCP = monodicalcium phosphate; DFP = defluorinated phosphate;
MSP = monosodium phosphate; TCP = tricalcium phosphate.
1
Volcanic MCP.
2
Non-volcanic MCP.
3
In MCP with 50–100% MCP.
M. Presto Åkerfeldt, S. Stiernström, K. Sigfridson et al. Animal 17 (2023) 100819
5

that may make specific diet-dependent endogenous losses and
higher total endogenous losses. In the present study, however,
the P-free basal diet was based on corn starch and could be
assumed to be comparable with that of Petersen and Stein
(2006). The estimated TTTD of P in PCP and MCP in the present
study were higher than the ATTD, which is in agreement with
the results of Petersen and Stein (2006). However, both the ATTD
and TTTD of P in PCP were lower compared with the other tested
feed phosphates in the literature (Table 7). Large variations in P
digestibility both among and between different P sources have
however been reported by others and are likely due to both differ-
ences in experimental set-up and quality of P-sources (Bikker et al.,
2016; Rodehutscord et al., 2017; Trairatapiwan et al., 2018). There-
fore, it has been suggested that comparisons between sources
mainly should be made within studies (Rodehutscord et al., 2017).
Due to diet composition, it was not possible to estimate the Ca-
digestibility for the individual P sources MCP and PCP, only for the
complete diets in the present study. The present chicken study
showed no difference in Ca-digestibility between the diets with
MCP and PCP inclusion. The basal diet in the chicken study without
the addition of MCP and PCP had an IAD of Ca of 59% and the diets
with MCP and PCP inclusion ranged between 54.7 and 58.1%. In
comparison, Bikker et al. (2016) estimated IAD of Ca to 67% in their
low P basal diet and to 66%, 60%, 64% and 37% for diets with MCP,
DCP, monodicalcium phosphate and defluorinated phosphate,
respectively. However, many factors such as Ca-source, particle size
and Ca-level might affect Ca digestibility (Kim et al., 2018) which
makes it hard to make direct comparisons between studies.
The ATTD of Ca for pigs was lower in the PCP than MCP diet (58.5
vs 71.3%). For pig studies, the ATTD of Ca in diets used by Lopez Diaz
(2020) was 52% for volcanic MCP and 60% for non-volcanic which is
similar to the ATTD of Ca of 58.5% in the PCP diet in the present
study. The majority (96.8%) of Ca in the PCP diet originated from
PCP and the diet digestibility is therefore likely a good estimation
of the ATTD of Ca in PCP. The Ca-digestibility of 71.3% for pigs on
the MCP diet in the present study is slightly higher than Lopez Diaz
et al. (2020) reported, but is on the other hand slightly lower than
76% that is reported for MCP by Kwon and Kim (2017). In compar-
ison, Kwon and Kim (2017) also reported ATTD of Ca in DCP to 74%,
monodicalcium phosphate to 72%, monosodium phosphate to 67%
and tricalcium phosphate to 64%.
Conclusion
In conclusion, this study shows that recycling of a clean and safe
phosphorus product can be used as a feed phosphate in diets to
monogastric animals. The amount of digestible P in PCP for chick-
ens do not differ from conventional MCP, whereas for pigs, it was
lower than reported for conventional MCP, however, in the same
range as literature data for conventional DCP and tricalcium phos-
phate. The use of a recycled P source has the potential to be used as
a viable alternative to other common sources of P.
Ethics approval
The study was approved by the Uppsala Ethics Committee on
Animal Research (ethics approval numbers 5.8.18-10572/2019 for
the chicken study and 5.8.18-03495/2021 for the pig study), which
is in compliance with EC Directive 86/609/EEC on animal studies.
Data and model availability statement
Data are deposited in an official repository at SLU, Dept. of Ani-
mal Nutrition and Management, Swedish University of Agricultural
Sciences, Box 7024, 750 07 Uppsala, Sweden. Access rights to data
and processes are available to reviewers upon request.
Author ORCIDs
M. Presto Åkerfeldt: https://orcid.org/0000-0002-0616-7763.
E. Ivarsson: https://orcid.org/0000-0001-9813-6915.
Author contributions
M. Presto Åkerfeldt: Data curation, Investigation, Methodology,
Formal analysis, Software, Validation, Writing – original draft,
Writing – review & following; S. Stiernström: Conceptualisation,
Funding acquisition, Project administration, Visualisation, Writing
– review & following. K. Sigfridson: Methodology, Formulation,
Software; E. Ivarsson: Conceptualisation, Funding acquisition, For-
mal analysis, Methodology, Data curation, Software, Formal analy-
sis, Writing – original draft, Writing – review & following; All
authors have read and agreed to the published version of the
manuscript.
Declaration of interest
The authors report no conflict of interest.
Acknowledgements
The authors gratefully thank the staff in the pig and chicken sta-
bles at the Swedish Livestock Research Center, SLU, Uppsala. The
authors also would like to thank all people involved at Lantmännen
Lantbruk, for optimising and producing the test feed used in this
study.
Financial support statement
This work was supported by Lantmännen Research foundation
[grant number 2020H002].
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