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Journal of Food Engineering 73 (2006) 379–387 www.elsevier.com/locate/jfoodeng

The effect of citrate on calcium phosphate deposition from simulated milk ultrafiltrate (SMUF) solution Roxane Rosmaninho *, Luı´s F. Melo LEPAE, Departamento de Engenharia Quı´mica, Faculdade de Engenharia da Universidade do Porto, Rua Dr. Roberto Frias, 4200-465 Porto, Portugal Received 27 September 2004; accepted 5 February 2005 Available online 7 April 2005

Abstract As has been widely reported, different calcium phosphate phases can be formed in solution depending on several physical-chemical aspects like the concentration of free calcium and phosphate ions, pH of the solution, temperature and the presence of interfering ions. The present work aims at studying the effect of pH and of citrates on the precipitation of calcium phosphate in a solution that simulates the mineral composition of milk (SMUF), as well as the subsequent effect on the deposition on stainless steel surfaces. The different calcium phosphate species formed during heating at different pH values and in the presence or absence of citrate were characterized by scanning electron microscopy, X-ray microanalysis and X-ray diffraction. Their fouling behaviour was characterized according to the amount of deposit formed on stainless steel surfaces and to the deposits resistance to removal by hydrodynamic shear forces. The absence of citrate was responsible for the decrease in the solution pH and for the formation of a crystalline dicalcium phosphate dihydrate structure with a deposited mass which was almost twice the one obtained in the presence of citrate. 2005 Elsevier Ltd. All rights reserved. Keywords: Milk fouling; Citrate; Hydroxyapatite; Dicalcium phosphate dihydrate

1. Introduction Fouling in milk processing is a complex process because it involves several simultaneous phenomena associated with protein aggregation and subsequent deposition and mineral salts deposition, the latter mainly caused by calcium phosphate (Jeurnink, Walstra, & deKruif, 1996). It has not yet been clarified whether calcium phosphate fouling is due to deposition of particles which have been formed in the bulk, or due to direct crystallization/precipitation on the surface (Andritsos, Yiantsios, & Karabelas, 2002). Therefore, the fouling process must be analysed not only in terms of deposit

*

Corresponding author. Fax: +351 22 5081449. E-mail address: [email protected] (R. Rosmaninho).

0260-8774/$ - see front matter 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jfoodeng.2005.02.017

adhesion and growth but also according to what is happening in the bulk solution. The most widely used test solution in milk mineral deposition studies is called simulated milk ultrafiltrate (SMUF) which was first described by Jenness and Koops (1962). It is a simplified milk system which constitutes, so far, the best way to evaluate the role of the different milk mineral components on the overall milk fouling behaviour. Due to the use of this simplified system more is now known about the mechanisms of fouling of the different milk components but there are still remaining some key scientific problems related to the poor understanding of the role of some interfering ions such as citrate (also present in SMUF) on the precipitation behaviour of calcium phosphate under different pH values. Calcium phosphate formation by precipitation from solution is determined by two mechanisms which only

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occur under supersaturated solutions: (i) nucleation and (ii) crystal growth. The latter is composed of several steps, starting with transport of ions from the bulk solution to the nuclei surface, followed by adsorption on energetically favourable sites. The formation of calcium phosphate nuclei and, afterwards, the precipitation phenomenon are only observed after a defined concentration of the correspondent ions in solution is reached. That concentration, the solubility, varies with the overall solution conditions. In solutions containing calcium and phosphate, a number of calcium phosphate phases may be formed (Fig. 1), depending mainly on the pH and calcium concentration. As a result of that, calcium phosphate precipitation will depend on the phase closest to saturation at the prevailing solution conditions. However, in environments which mimic milk, urine or other natural biological solutions, the interactions caused by other ions are significant and the solubility isotherms can only be used as a starting point for prediction of the forming phase. The goal of this work is to obtain advances on the interactions between citrate ions and calcium phosphate in simulated milk solutions, in order to better understand the formation of unwanted deposits on surfaces and to design appropriate cleaning strategies. There are a wide range of calcium phosphate phases that may precipitate, most likely as precursors to hydroxyapatite (HAP), as defended by several authors (House, 1999; Liu, Sethuraman, Wu, Nancollas, & Grynpas, 1997; Milev, Kannangara, & Ben-Nissan, 2003; van Kemenade & de Bruyn, 1987; Visser & Jeurnink, 1997), namely dicalcium phosphate dihydrate or brushite (DCPD), octacalcium phosphate (OCP), tricalcium phosphate (TCP) or amorphous calcium phos-

Fig. 1. Calcium phosphate solubility isotherms (Vereecke and Lemaitre, 1990).

phate (ACP). It is well established that kinetic factors may be of great importance in determining the characteristics of the phases formed during the precipitation process together with equilibrium considerations. In other words, what is thermodynamically the most stable phase may not be the one which precipitates first because its precipitation kinetics is slower. The formation of the different calcium phosphates species can consequently be explained by kinetic, thermodynamic or solubility effects, or on the other hand be the result of the interactions with other substances present in solution. Little is currently known about the conditions or levels of supersaturation necessary to produce precipitation in the last case, more precisely to overcome the effect of organic ligands, because not much is yet known about the interactions between those organic molecules and the calcium phosphate compounds formed in solution. A number of kinetic studies have attempted to establish the specific conditions for the formation of each precursor phase, most of them having been carried out under the constant composition method (Koutsoukos, Amjad, Tomson, & Nancollas, 1980). Ions such as magnesium have also been reported as important inhibitors for the precipitation of certain phases, by forming chemical complexes with the newly formed surfaces, blocking further precipitation (Abbona & Franchiniangela, 1990). Some studies do exist assessing the effect of organic ligands like citrate and acetate on the precipitation of dicalcium phosphate dihydrate (DCPD), octacalcium phosphate (OCP) and hydroxyapatite (HAP). In seeded solutions, they all reported inhibition of hydroxyapatite precipitation by adsorption of the organic molecules on active growth sites of the seeding material, resulting in the formation of phospho-citrate complexes (van der Houwen & Valsami-Jones, 2001). This inhibition effect of citrate on calcium phosphate kinetics was first presented in an earlier study, at the time concerned with the inhibition effect on the transformation of OCP into any other more stable crystalline form (Sharma, Johnsson, Sallis, & Nancollas, 1992). Some work concerning the role of citrate on calcium phosphate precipitation from a SMUF solution was also presented in a recent publication by Andritsos et al. (2002) at pH values and temperatures different from those tested in the present paper and whose conclusions will be discussed later. Although considerable work has been done on calcium phosphate precipitation and on the preferential precipitation phases, the majority of those studies was carried out in low ionic strength solutions, mainly composed of calcium and phosphorous. In the present work, the study of the different calcium phosphate phases formed under heating treatment and in the presence of citrate was evaluated for a solution which simulates the mineral composition of milk. The final goal is to contribute to the understanding of the fouling process in milk pasteurization processes.


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2. Materials and methods The experimental work described here was focused on the effect of citrate on the precipitation behaviour of calcium phosphate from a milk simulating solution upon heating. Special attention was given to: (i) the type of calcium phosphate structures precipitated in the bulk; (ii) the type of deposit formed on stainless steel surfaces. To detail the effect of citrate on the deposition behaviour, two different solutions were used: (1) SMUF solution (containing citrate), prepared with deionised water and appropriate amounts of the reagents (analytical grade), following the recipe of Jenness and Koops (1962), whose stequiometrical final composition is summarized in Table 1. The solution had a pH of 6.30 after preparation and was adjusted to 6.80 with KOH or to 6.15 with HCl as desired. (2) modified SMUF solution (without citrate). This last solution had a pH of 6.15 immediately after preparation and no pH adjustment was performed in this case. The fouling behaviour of the different solutions was evaluated by performing deposition experiments on stainless steel surfaces (316 2R finish) and evaluating: (i) the amount of deposit formed on the surface by weighing (analytical balance AND GR-200); (ii) the structure of the deposits formed on the surface by scanning electron microscopy observation (JEOL JSM6301F), (iii) their chemical composition by X-ray microanalysis (Noran Voyager) and (iv) the percentage of deposit mass detached from the surface by hydrodynamic forces at the temperature and pH used during the deposition stage. Before each deposition experiment, the stainless steel samples used as deposition surfaces were cleaned with a commercial detergent (RBS35 from RBS Chemical Products) according to the following procedure: (1) samples were immersed in a 2.0% w/v detergent (RBS35) solution in distilled water at 65 C for 5 min; (2) rinsed with distilled water at 65 C for 5 min and (3) rinsed with distilled water at 20 C. The experiments were performed with a rotating disk apparatus (Fig. 2) to study the fouling behaviour of cal-

Table 1 Composition of the SMUF solution Reagents

Concentration in solution (mM)

KH2PO4 K3 citrate Æ H2Oa Na3 citrate Æ 2H2Oa K2SO4 K2CO3 KCl CaCl2 Æ 2H2O MgCl2 Æ 6H2O

11.61 3.70 6.09 1.03 2.17 8.05 8.98 3.21

a

Citrate ¼ C6 H8 O 3.

Fig. 2. Schematic representation of the rotating disk apparatus.

cium phosphate under controlled hydrodynamics and temperature. The apparatus is composed of a thermostatic vessel where the solution is contained, temperature being controlled by a hot water bath and by a hollow cone containing heated silicone oil. Deposition occurs on the stainless steel plate attached to the bottom of the cone. The plate/cone set is allowed to freely rotate in the solution, the Reynolds number of the system being controlled by its rotating speed. In the present work, the rotating speed during deposit formation was 150 rpm (laminar regime, Re = 4.6 · 104). Opposed to the constant composition method which has been more commonly used in crystallization experiments (Koutsoukos et al., 1980; Nancollas & Wu, 2000), during the present experiments the pH of the solutions was allowed to decrease freely without any kind of control, as it would occur in real milk heating processes. The stainless steel samples were attached to the heating cone and then introduced in the foulant solution contained in the heated vessel. The test solutions (modified SMUF and SMUF at pH 6.80) were heated, at a defined heating rate, to the desired deposition temperature (45 C). The cone/plate set was kept rotating for 120 min to allow the formation of a stable deposit on the stainless steel plate. After that time, the set was gently removed from the solution. The plate was detached from the cone, dried at air and the amount of deposit obtained was weighed. Detailed analyses of the deposits were made at this point. The foulant solution was then replaced by distilled water adjusted to the same pH and temperature of deposition. The set composed by the cone and the fouled plate was introduced in the water and was rotated at increasing speeds of 165, 180, 210, 240, 270 and 300 rpm. Each of these rotating experiments were carried out for 5 min. After each experiment, the sample

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was removed, dried and weighed in order to assess the total amount of deposit detached from the surface. Particle formation in the bulk can be detected by the increase in the turbidity of the solution (Andritsos et al., 2002; Visser, 1999) and by a decrease in the pH value (Christoffersen, Christoffersen, & Kibalczyc, 1990). pH variation during heating was measured (WTW Inolab pH level 3) and turbidity was followed using a UV/ VIS spectrophotometer (Philips PU8620) at a wavelength of 610 nm, taking one sample for every temperature degree increase. As soon as the solution became turbid and at the end of the deposition experiment (after 120 min at constant temperature), part of the solution was vacuum filtered and the deposit was examined with scanning electron microscopy and characterized by X-ray microanalysis and X-ray diffraction (XPert Pro PANalytical diffractometer with a Cu X-ray tube) to define their crystallinity. Calcium concentration of the different solutions at the beginning of the experiments was measured using a selective electrode (WTW-D82362 Weitheim).

3. Results and discussion

Abs (610 nm)

As mentioned before, the solutions with and without citrate presented different pH values immediately after preparation. The experiments performed with SMUF solution at different pH (6.15, 6.30 and 6.80) aimed to investigate possible pH effects on the deposition process. The difference in the pH of the solutions prepared with or without citrates, keeping all the remaining components constant, has already been described by other authors, although in a different but still exclusively mineral system, who discussed the synergetic role of citrate ions when raising the pH (Allie & Rodgers, 2003). Citrates are known to be calcium binders (Andritsos et al., 2002; Nancollas & Wu, 2000), the main consequence of their presence being the decrease of calcium free ions in solution. The concentration of free calcium ions in solution for the different solutions analysed is presented in Table 2. As can be easily verified in Table 2, the concentration of calcium ions in solution is similar for all the three SMUF solutions and much higher for the modified solu-

Table 2 Initial concentration of free calcium in solution Solutions Modified SMUF SMUF (pH 6.15) SMUF (pH 6.35) SMUF (pH 6.80)

tion which does not contain citrates. This was the first physical observation which seemed to confirm the complexing effect of calcium by the citrates and the fact that interactions could appear between citrate and all the other calcium compounds formed in solution. The logarithmic values of the calcium concentration were calculated and are presented in that table but will be used later on Fig. 9. The concentration of phosphorous is not presented since it is not influenced by the presence of citrates (van der Houwen & Valsami-Jones, 2001). Bulk precipitation was initiated when supersaturation occurred as a result of the increase temperature due to heating. In order to know the temperature at which bulk precipitation starts, the heating effects on the solutions were monitored by spectroscopy at 610 nm (Fig. 3). The initiation of particle formation was detected at different temperatures depending on the solution. A delay in this starting point for the SMUF solutions can be explained by the fact that citrates removed the available calcium from solution and consequently supersaturation according to calcium phosphate was only achieved at higher temperatures. The modified SMUF solution became turbid at a lower temperature than the others, at about room temperature. In this situation, all the calcium is consumed to form calcium phosphates. On the other hand, all the non-modified SMUF solutions needed higher temperatures to acquire enough supersaturation for precipitation and in those cases, a decrease in the pH from 6.80 to 6.15 corresponds to an increase in the temperature at which precipitation starts from 45 to 70 C (Fig. 3). This suggests the existence of an alternative mechanism with inhibition of nucleation and/or growth, due to citrate binding onto active growth sites of the newly formed nuclei. In such a case, growth of the nuclei is inhibited until there is enough supersaturation of calcium in solution for precipitation to occur. Some previous studies also found that the presence of citrate delays the occurrence of crystals and reduces the crystallization rate which slows down the transformation of these particles into a more stable calcium

Calcium concentration (mM)

Log (calcium concentration [M])

4.25 0.75 0.70 0.48

2.38 3.12 3.15 3.30

0.2

modified SMUF

0.18

SMUF pH 6.15

0.16

SMUF pH 6.35

0.14

SMUF pH 6.80

0.12 0.1 0.08 0.06 0.04 0.02 0 0

20

40

T(ºC)

60

80

100

Fig. 3. Turbidity evolution of the solutions during heating.

R. Rosmaninho, L.F. Melo / Journal of Food Engineering 73 (2006) 379–387 modified SMUF SMUF pH 6.80

7 6.8 6.6

beginning of turbidity

pH

6.4

beginning of turbidity

6.2 6 5.8 5.6 5.4 5.2 5 20

25

30

35

40

45

50

T (ºC)

Fig. 4. pH decrease with heating of modified SMUF and SMUF at pH 6.80.

phosphate form (van der Houwen, Cressey, Cressey, & Valsami-Jones, 2003). Fig. 4 shows in more detail the case of modified SMUF (pH of 6.15) and non-modified SMUF at pH 6.80, where the increase in turbidity is also related to a decrease in pH. The precipitation of calcium phosphate from solution is a base uptake process because of the dissociation of the hydrogen-containing phosphate species present. In a given precipitation system without base addition, the pH value will decrease during the precipitation reaction. For this reason, the decrease in pH can be used as a measure of calcium phosphate particle

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formation in solution. Despite similar changes in turbidity, the decrease in pH is different depending on the solution: 5 C above the temperature at which turbidity starts the pH of the modified SMUF decreased by 0.4 units, while for the same temperature variation a decrease of only 0.1 units was found in SMUF. This variation on pH decrease can also be related to the formation of different calcium phosphate species as different species have different alkalinities. To verify which structures were being formed under the different conditions considered in this work, the solutions were filtered after reaching an optical density of 0.2 and the precipitates were analysed by X-ray microanalysis and observed by scanning electron microscopy (SEM). All the precipitates were mainly composed of calcium phosphate, with a very small amount of magnesium or sodium which is not surprising since these ions were present in the initial solutions (Fig. 5). According to the pictures in Figs. 6 and 7, obtained by scanning electron microscopy (SEM), different calcium phosphate structures were formed depending on the composition and pH of the solution. Structures formed from SMUF at pH 6.80 (Fig. 6) consisted of spherical crystals held together in clusters similar to bunches of grapes, which had already been reported as characteristic of hydroxyapatite compounds (van

Fig. 5. X-ray microanalysis of the different precipitates formed on solution upon heating: (a) modified SMUF, (b) SMUF at pH 6.15, (c) SMUF at pH 6.30 and (d) SMUF at pH 6.80.

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Fig. 6. Calcium phosphate structures obtained from SMUF at pH 6.80: (a) 5000· amplification and (b) 50,000· amplification.

Fig. 7. Calcium phosphate structures obtained from SMUF at pH 6.15: (a) 5000· amplification and (b) 50,000· amplification.

Kemenade & de Bruyn, 1987; Visser & Jeurnink, 1997). The structure of the precipitates formed from SMUF at pH 6.15 was somewhat different: although also packed in a bunch of grape form, the individual spheres were bigger and showed a more irregular structure (Fig. 7) which had also been identified as hydroxyapatite in a non-crystalline form, more precisely in an intermediate stage between brushite and hydroxyapatite (Ferreira, Oliveira, & Rocha, 2003). A similar structure, although not presented here, was found for SMUF at pH 6.30. The most significant difference in structure and morphology was found for the precipitate formed from the modified SMUF solution, where calcium phosphate showed a plate-like shape typical of brushite (Fig. 8). According to the solubility isotherms of calcium phosphate (Fig. 1), the precipitating phase depends on the relation between the calcium concentration in solution and the pH. The different situations analysed in this work are presented in Fig. 9, considering the logarithmic values of calcium concentration in the solution. Calcium concentrations in the three SMUF solutions (points 2, 3 and 4 in Fig. 9) are much lower than that in the solution without citrate, as a result of calcium complexation promoted by the citrates (van der Houwen & ValsamiJones, 2001). The solution could be considered supersaturated according to hydroxyapatite and so the

Fig. 8. Calcium phosphate structures obtained from modified SMUF with 1500· amplification.

formation of hydroxyapatite precipitates could be expected. For the solution without citrates, where the calcium concentration in solution is higher and the initial pH is lower (point 1 in Fig. 9), the most probable precipitate was dicalcium phosphate dihydrate or brushite.


Fig. 9. Solubility isotherms for calcium phosphate and the different binomial calcium concentration in solution/pH for the solutions analysed: (1) modified SMUF, (2) SMUF pH 6.15, (3) SMUF pH 6.30 and (4) SMUF pH 6.80.

Similar results were also found by other authors who claimed that the presence of citrate in solution was also responsible for lowering the supersaturation in terms of brushite (Allie & Rodgers, 2003). The identification of the structures involved and its crystallinity can be seen in detail in Fig. 10 containing the X-ray diffraction diagrams of the precipitates. All the precipitates formed from SMUF showed very similar patterns of poorly crystalline hydroxyapatite, with no evidence of any other phase being present. The precipitates formed from the solutions at pH of 6.15 (Fig. 10c) and 6.30 (Fig. 10b) showed an amorphous structure with a small peak in early development, which is characteristic of hydroxyapatite, while the one from the SMUF

385

solution at pH 6.80 (Fig. 10a) showed a more structured hydroxyapatite compound, although not yet crystalline. On the other hand, the precipitate formed from modified SMUF was brushite in a perfect crystalline form (Fig. 10d). The fact that the pH of the solution has a considerable effect on the type of calcium phosphate structure formed was confirmed by the results presented before. The formation of the same calcium phosphate phase in all three SMUF solutions but in different crystallinity stages leads to the conclusion that different pH values with similar ionic concentration affect the crystallinity instead of the nature of the chemical compound formed. The absence of citrate (modified SMUF) showed an even stronger effect on the precipitation process: the modified SMUF produced a precipitate composed of brushite in a totally crystalline phase, whereas for the same pH the non-modified solution formed an amorphous hydroxyapatite phase. The relationship between the formation of different structures in the bulk and the build up of calcium phosphate deposits on stainless steel surfaces was also studied. After 120 min of deposition, the deposits formed on the stainless steel surfaces were analysed by scanning electron microscopy and X-ray microanalysis. It could be concluded that the structure of the deposits was determined by the particles present in the bulk, as can be checked in Fig. 11a for SMUF solution at a pH of 6.80 and in Fig. 11b for modified SMUF. The first type of deposit was composed of an initial layer of hydroxyapatite aggregates, on top of which other aggregates with a similar sphere-like structure were formed, developing a multilayer deposit packed in a grape-like shape form. The second type of deposit

Fig. 10. X-ray diffraction diagram for the different calcium phosphate precipitates formed: (a) SMUF pH 6.80, (b) SMUF pH 6.30, (c) SMUF pH 6.15 and (d) modified SMUF.

386


Fig. 11. Deposits formed on 2R stainless steel surfaces after 120 min of deposition: (a) SMUF pH 6.80 and (b) modified SMUF.

Table 3 Mass of deposit formed on 2R stainless steel surfaces after 120 min deposition experiments and percentage of deposit removal in cleaning experiments (r is the standard deviation) Solutions

Mass of deposit (g/m2)

Percentage of removal (%)

Modified SMUF (without citrate) SMUF (pH 6.80) (with citrate)

5.5 (r 0.2) 2.5 (r 0.1)

78.4 (r 0.9) 76.1 (r 0.2)

(Fig. 11b) showed a less defined first layer where the plate-like structures seem to be laid on. The removal experiments suggested that they were in fact adhered to the surface. The amount of deposit formed in each case (after 120 min deposition) and the amount of mass deposit removed after the removal experiment cycle are presented in Table 3. Under the same deposition conditions, the mass of deposit formed was the double for the brushite case (without citrate). Although opposed to what has been reported earlier by Andritsos et al. (2002), this could be expected since the structures formed in the bulk, the ones responsible for the build up of the deposit, were much larger in the brushite case. It was interesting to find that under the same hydrodynamic conditions, a similar percentage of mass was removed from the surface, independently of the deposit morphology and composition.

4. Conclusions In this work, the effect of citrates on the precipitation of calcium phosphate from an aqueous solution which simulates the mineral composition of milk (SMUF) was evaluated. Three main parameters were affected by the presence or absence of citrates: (1) the pH of the solution before precipitation was lower in the absence of citrates; (2) the calcium phosphate phase that

precipitated when heating the solution changed from hydroxyapatite in the presence of citrates to brushite in the absence of citrates and (3) the deposits that build up on stainless steel surfaces in each case had different morphology and total mass but showed similar resistance to detachment when submitted to similar hydrodynamic forces. This last conclusion is especially important when choosing the cleaning strategies to apply in fouled heat exchangers, since it means that although a greater percentage of the brushite deposit (absence of citrate) can be removed from the surface, the remaining deposit mass is higher than in the case of hydroxyapatite (presence of citrate).

Acknowledgments The authors gratefully acknowledge the financial support of the MODSTEEL Project (The European Commission, DG Research, Growth Programme, Contract no. G5RD-CT-1999-00066) and the SIMUMILK Project (FCT, Portuguese Science Foundation, POCTI/ QUE/47654/2002).

Appendix A. Nomenclature and units T Re

temperature (C) Reynolds number (dimensionless) 2

Re ¼ X tx h5 104 i for laminar regime X plate dimension (m) x angular velocity (rad/s) m kinematic viscosity of the fluid (m2/s) SMUF simulated milk ultrafiltrate HAP hydroxyapatite DCPD dicalcium phosphate dihydrate or brushite [CaHPO4 Æ 2H2O] OCP octacalcium phosphate [Ca4H(PO4)3 Æ 2.5H2O]


TCP ACP

tricalcium phosphate [Ca3(PO4)2] amorphous calcium phosphate

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