As phosphorus (P) is an essential inorganic nutrient for pigs playing a crucial role in various biological processes and bone growth, providing pigs with a sufficient quantity of P is essential. However, due to the high cost of P sources and concerns about environmental pollution (Han et al., 2001), P concentrations in swine diets should be precisely formulated to meet the requirements. Numerous studies have been conducted to accurately determine the P requirement and digestibility in pigs (Adeola et al., 2015; Hong and Kim, 2021; Kong et al., 2021). Traditionally, the availability of P has been determined using the relative bioavailability of P (Cromwell, 1992; NRC, 1998). However, relative bioavailability values have limitations for feed formulation due to non-additivity in mixed diets (NRC, 2012). Therefore, the concept of a standardized digestibility assay for P has been adopted, similarly to amino acids (NRC, 2012), allowing for a more precise estimation of P utilization in swine nutrition.

With the adoption of the standardized digestibility assay, P digestibility has been evaluated at the total tract level because it is easier to do so for determining P digestibility than at the ileal level (Lee and Stein, 2023). Several studies have shown no difference between the ileal digestibility and the total tract digestibility of P in pigs (Dilger and Adeola, 2006; Fan et al., 2001; Zhang et al., 2016). Furthermore, Jongbloed et al. (1992) documented even negative hindgut disappearance (HD) of P in pigs. Consequently, the hindgut absorption of P has often been considered negligible in pigs. However, some studies have reported the presence of HD of P, which is calculated by subtracting the ileal digestibility value from the total tract digestibility value, under certain dietary conditions or physiological stages of pigs. When pigs are fed a diet with a low calcium (Ca)-to-P ratio (Ca:P; Liu et al., 2000) or a corn-soybean meal (SBM)-based diet (Liu et al., 2017), the positive HD of P has been reported. Similarly, positive HD of P in pigs was observed when pigs reached a body weight (BW) greater than 60 kg (Liu et al., 2018). These inconsistent findings regarding the HD of P suggest that the large intestine may have the ability to utilize P under specific environmental conditions. Nevertheless, information on HD of P is limited due to the difficulties in its determination and interpretation (Son et al., 2023). Therefore, the present study aimed to investigate the difference between the ileal digestibility and the total tract digestibility of P in pigs using published data and investigate the factors that could affect HD of P in pigs with a hypothesis that the total tract digestibility of P is greater than ileal digestibility of P in pigs.

The initial BW of pigs ranged from 10.0 to 104.8 kg (Table 1). The diets used in the present study had total P concentrations ranging from 0.09% to 0.91% and phytate-P concentrations from 0.02% to 0.66% on a DM basis. The AHD and SHD of P varied from −23.1% to 39.6% and −22.8% to 39.8%, respectively.

The ATTD of P was greater than the AID of P (P = 0.035; Table 2). Additionally, the STTD of P was greater than the SID of P (P = 0.019). The AHD of P was positive in 116 out of 156 observations (Table 3). The Chi-square analysis indicated that the supplementation of inorganic P sources tended to result in a higher occurrence of a positive value for AHD of P (P = 0.099). In addition, there was a relationship between the AHD of P and BW of pigs (P = 0.027). When the BW of pigs was below 30 kg, the occurrence of positive AHD of P was lower. However, as the BW of pigs increased, the occurrence of positive AHD of P increased.

Similarly, the SHD of P was positive in 118 observations out of 156 total data (Table 4). Based on the Chi-square analysis, the supplementation of inorganic P sources tended to result in a higher occurrence of a positive value for SHD of P (P = 0.079). The BW of pigs also tended to be associated with the occurrence of positive value in SHD of P (P = 0.061) in that the occurrence of positive value in SHD of P was lower when the BW of pigs were below 30 kg whereas the occurrence of positive value in SHD of P increased as the BW of pigs increased at over 30 kg.

Regression analyses of the SHD of P against SID of P in pigs indicated that the SHD of P decreased as the SID of P increased in pigs (Fig. 1; r² = 0.174). The SHD of P was increased with standardized ileal undigestible P when expressed as g/d (Fig. 2; r² = 0.212). The standardized hindgut undigestible P increased with Ca intake when expressed as g/d (Fig. 3; r² = 0.777).

To determine standardized P digestibility, the total tract digestibility has been employed due to its practicality and cost-effectiveness compared with the ileal digestibility (Lee and Stein, 2023). Several studies reported no difference between ileal and total tract digestibility of P in pigs (Dilger and Adeola, 2006; Fan et al., 2001; Zhang et al., 2016), and thus, the total tract digestibility has been used with the assumption of equivalence between ileal and total tract digestibility of P in pigs. Consequently, the contribution of the large intestine to P digestion and absorption in pigs has been traditionally considered negligible. However, other studies have reported the existence of absorption of P in the large intestine of pigs. Liu et al. (2000) reported that P was absorbed in the large intestine of 123-kg pigs fed corn-SBM-based diets. Similarly, Son et al. (2023) observed a 10.5% AHD of P when pigs were fed a wheat-SBM-based diet containing 20% wheat bran and dicalcium phosphate at 0.1%, although no linear or quadratic effects of wheat bran on AHD of P were observed. Fan et al. (2001) proposed that the absorption of P in the large intestine of pigs primarily involves reabsorption of endogenous losses of P, rather than ingested P, resulting in zero P retention in the large intestine. Despite numerous studies on P utilization in the hindgut of pigs, controversies still exist (Liu et al., 2000, 2017; Son et al., 2023). In the present study, the greater STTD than SID of P in pigs was observed, consistent with previous findings (Johnston et al., 2004; Liu et al., 2017, 2018), suggesting net absorption of P in the hindgut of pigs.

The varied results of interactions between the use of phytase or the use of inorganic P sources and the HD of P were unexpected (Tables 3 and 4), considering that both phytase and inorganic P sources would result in a reduced amount of undigested P entering the hindgut of pigs. Supplemented phytase primarily hydrolyzes phytate-P in the stomach and proximal small intestine before reaching the jejunum (Park and Adeola, 2023). The phosphate liberated from phytate by supplemented phytase is readily absorbed before reaching the end of the ileum through passive diffusion via tight junctions and active transport through sodium-dependent phosphate transporters in the small intestine (Sabbagh et al., 2011). Likewise, when inorganic P sources are supplemented, the inorganic P sources are solubilized by the high acidity in the stomach and are readily absorbed in the small intestine (Goss et al., 2007). Therefore, the digestion and absorption of P in diets with relatively high inorganic P concentrations, in comparison to diets lacking inorganic P sources, are completed before reaching the end of the ileum, as is the case with phytase supplementation (Zhai et al., 2022). This leads to relatively small amounts of undigested P entering the hindgut of pigs. Consequently, the HD of P may be restricted when either phytase or inorganic P sources are used, as the HD of P depends on the quantity of undigested P entering the hindgut. However, the results of the Chi-square tests were not consistent with the linear relationships between the SHD of P and the SID of P or standardized hindgut undigested P in the present study. Although the rationale for this discrepancy remains unclear, this could be attributed to the classification criterion, which depends on the presence or absence of phytase or an inorganic P source rather than their concentration levels, based on the dichotomous characteristics of the Chi-square analysis. For instance, even if there is a small amount of phytase and inorganic P source enough to exhibit a positive HD of P in the diet, it can be classified as the presence of phytase or an inorganic P source in the Chi-square test. Alternatively, the inconsistency between the regression analyses and the Chi-square tests could be partially explained by different diet constituents such as the concentration of phytate or the physiological conditions of pigs.

Several studies showed that phytase or inorganic P supplementation reduces the HD of P. Johnston et al. (2004) reported that AHD of P decreased from 9.1% to 5.8% when pigs with a BW of 53 kg were fed a diet supplemented with phytase and monocalcium phosphate as an inorganic P source. Furthermore, Bruce and Sundstøl (1995) reported that the diet with both monocalcium phosphate at 0.55% and phytase at 375 FTU/kg had less AHD of P (2.7%) compared with the diets with phytase at 750 FTU/kg (AHD of P = 6.3%), the diet with monocalcium phosphate at 1.11% (AHD of P = 7.3%), or the diets without inorganic P source or phytase (AHD of P = 9.4%). However, Mok et al. (2013) reported that there was no significant difference when comparing pigs fed a corn-SBM-palm kernel meal-based diet supplemented with phytase at 1000 FTU/kg and those without phytase supplementation (9.2% vs. 12.1%). Additionally, when 27.8-kg pigs were fed a corn-SBM-based diet with increasing dicalcium phosphate, no response of AHD of P was observed (Liu et al., 2017). Therefore, inconsistency in the magnitude of supplementation of phytase or inorganic P sources in diets among the published studies necessitates further research to elucidate on the impact of phytase and inorganic P source supplementation on the extent of HD of P in pigs.

The observed interaction between BW of pigs and HD of P can be explained by the findings of Liu et al. (2018), who demonstrated that pigs above 60 kg BW exhibited HD of P due to their greater capacity for hindgut digestion and absorption of P compared with pigs weighing 25 kg. This can be attributed to the increasing length of the large intestine in pigs as their BW increases, resulting in a longer residence time of digesta, and thus, the potential of absorption by the host or microbial fermentation in the large intestine may increase (Noblet and Shi, 1993, 1994). Finishing pigs have a greater potential for nutrient digestion and absorption or fermentation due to their longer gastrointestinal length and retention time compared with nursery or growing pigs (Noblet and Shi, 1994). In this manner, pigs with higher BW may exhibit a greater digestion capacity for P in the hindgut, leading to greater absorption or fermentation in the hindgut.

Moreover, the HD of P in pigs, which is dependent on BW, may be influenced by the diet composition. During the nursery stage of pigs, it is common to use animal-derived feed ingredients that contain greater amount of digestible P compared with P sources originated from plants (Kong et al., 2021). Phosphorus in animal sources is highly digestible compared with plant-derived P and may be readily absorbed before reaching the end of the ileum, which can result in low HD of P. In such cases, the HD of P may be limited regardless of the length of the gastrointestinal tract. On the other hand, the inclusion of fibrous sources such as wheat bran or palm kernel meal in the diet during the growing stage of pigs is common and may lower the digestibility of P until the ileum due to the shorter transit time in the gut due to the increased peristalsis by fiber fraction (Nortey et al., 2007). This can lead to a larger amount of P entering the hindgut, potentially resulting in the occurrence of HD of P. However, the influence of dietary fiber on the amount or proportion of P entering the large intestine was not observed in the present study. In the older pigs with a greater daily feed intake, the increased P intake can also lead to a larger amount of P entering the hindgut, thereby increasing the occurrence of HD of P (Liu et al., 2018).

Calcium may influence the HD of P in pigs. It is widely recognized that an excessive dietary Ca concentration or high Ca:P in diets can lead to reduced P digestibility in pigs (Klein et al., 2023; Lee et al., 2020; Stein et al., 2011). Despite the variations in feeds used in this meta-analysis, a strong linear relationship between Ca intake and standardized hindgut undigested P was observed. This suggests that large amount of Ca intake disrupts P absorption, extending this effect to the hindgut of pigs. Previous studies by Stein et al. (2011) and Lee et al. (2020) reported that increased Ca intake in the form of Ca carbonate resulted in a linear reduction in the ATTD of P in growing pigs and gestating sows, respectively. These studies discussed the potential for Ca to bind with P in the gastrointestinal tract of pigs, forming a Ca–P complex that is less readily digested and absorbed. Although this phenomenon has not been fully elucidated, it can be partially explained by the lower solubility of Ca–P complexes, such as Ca phosphate, in the lower gastrointestinal tract of pigs (Lee et al., 2020; Stein et al., 2011). Whereas Ca is mainly absorbed in the duodenum, P is mainly absorbed in both the duodenum and jejunum in pigs (Hoag and Dharmarajan, 2021). If excessive Ca is included in the diets, the unabsorbed inorganic form of P, phosphate, may combine with undigested Ca, resulting in the formation of a Ca-phosphate complex in the jejunum and ileum of pigs. Because the solubility of Ca-phosphate complex is maximized at a pH less than 3.0 such as the stomach, the solubility of Ca-phosphate complex sharply increased as the pH decreased from 6.0 to 2.0 (Goss et al., 2007). Because the pH in the duodenum, the jejunum to ileum, and the cecum to colon is from 3.1 to 5.5, from 5.6 to 6.0, and from 6.1 to 7.0, respectively (Roura et al., 2023), when Ca absorption ends in the duodenum, undigested Ca and P may form a Ca–P complex, and the solubility of Ca–P complex is further decreased due to the relatively high pH in the terminal small intestine and in the large intestine of pigs. This inference is supported by the results of Hoag and Dharmarajan (2021) who reported that Ca-salts inhibit P absorption, and therefore, a high Ca intake has the potential to bind P in the gastrointestinal tract. Moreover, it is also consistent with the results of increased absorption in the cecum and colon of pigs when the Ca:P is decreased from 1.5 to 1.0 in diets (Liu et al., 2000) and increased AHD of P when the ratio of Ca-to-digestible P decreased from 3:1 to 2:1 with decreasing limestone (Klein et al., 2023). As a result, the HD of P in pigs can be decreased or limited when a high Ca concentration is included in the diet.

Based on the findings in the present meta-analysis, the absorption of P in the large intestine is revealed. Smith et al. (1955) first suggested this phenomenon, identifying the cecum and colon as potential sites for regulating P homeostasis in pigs by observing the absorption of endogenous P losses using radioactive isotope P. Although the metabolic processes of P in the cecum and colon remain unclear, Seynaeve et al. (2000) suggested that phytates entering the hindgut are almost completely hydrolyzed by microbial enzymes allowing potential absorption of P in the cecum and the colon. For the absorption mechanism in the large intestine, Wubuli et al. (2019) reported the expression of genes for sodium-dependent phosphate transporters in the cecum and colon of 100-kg pigs, indicating that P can be transported from the lumen of the large intestine to the circulatory system. Although not in pigs, a sodium-dependent phosphate transporter was observed in the colon of rats (He et al., 2016). Further research is warranted to identify phosphate transporters in the hindgut of pigs.

In the present analysis, the ATTD of P was greater than the AID of P in 116 observations whereas the ATTD of P was less than the AID of P in 40 observations. In an extreme case for the negative HD of P, ATTD of P was 19 percentage unit less than AID of P in 30-kg pigs fed corn-SBM-based diets (Yang et al., 2020), indicating that a large quantity of endogenous P was secreted in the hindgut but the absorption of P in the hindgut was minimal. The specific reasons for negative HD of P remain unclear. However, Fan et al. (2001) suggested that a large portion of endogenous losses of P is reabsorbed in the large intestine. Moreover, the endogenous losses of P in the hindgut are relatively small considering that the basal endogenous losses of P at the end of the ileum are 177 mg/kg DM intake (Traylor et al., 2001) and those in the total tract are 190 mg/kg DM intake (NRC, 2012).

The present work determined hindgut disappearance of P for pigs using a Meta-analysis. The hindgut disappearance of P in pigs exists and is influenced by factors including the diet composition, the amount of P entering the large intestine, and the body weight. The determination of P digestibility at the total tract level may be appropriate for an accurate evaluation of P digestibility. Further research is warranted to investigate the metabolism of P in the large intestine of pigs.