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Compositional Changes of the Xiphoid Process and Costal Cartilage with Aging KAZUHIKO FURUTA,1 YOSHIYUKI TOHNO,*,2 SETSUKO TOHNO,2 YUMI MORIWAKE,2 TAKESHI MINAMI,3 YASUO TAKANO,4 CHO AZUMA,2 AND YOSHINORI TAKAKURA1 1

Department of Orthopedic Surgery and 2Laboratory of Cell Biology, Department of Anatomy, Nara Medical University, Kashihara, Nara 634-8521, Japan; 3Laboratory of Environmental Biology, Department of Life Science, School of Engineering and Sciences, Kinki University, Higashi-Osaka, Osaka 577-8502, Japan; and 4Department of Anatomy, Kochi Medical School, Nankoku, Kochi 783-8505, Japan Received August 21, 2002; Accepted November 10, 2002

ABSTRACT To elucidate compositional changes of the cartilage with aging, the authors investigated age-related changes of element contents in the xiphoid process and costal cartilage by inductively coupled plasma–atomic emission spectrometry. After the ordinary dissection by medical students was finished, the xiphoid processes and bilateral the fourth costal cartilages were resected and element contents were determined. The subjects consisted of 17 men and 9 women, ranging in age from 52 to 96 yr. No significant correlations were found between age and the content of elements, such as Ca, P, S, Mg, Na, Zn, Fe, and Si in the xiphoid process and costal cartilage, except for S in the costal cartilage, in which an extremely significant correlation was found. With regard to the relationships among element contents, the common finding that there were significant direct correlations both between Ca and P contents and between Ca and Mg contents, whereas there were significant inverse correlations both between Ca and S contents and between P and S contents obtained in the xiphoid process and costal cartilage. Index Entries: Xiphoid process; costal cartilage; cartilage; sulfur; calcium; phosphorus; aging. *Author to whom all correspondence and reprint requests should be addressed. Biological Trace Element Research

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INTRODUCTION To elucidate compositional changes of the cartilage with aging, the authors previously investigated age-related changes of element contents in the intervertebral disk (1), pubic symphysis (2), meniscus (3), articular disk of the temporomandibular joint (4), and trachea (5). There are many reports (6–13) on calcification or ossification of the costal cartilage and xiphoid process. However, little work has been done to study the relationships among elements in the cartilages. Therefore, the authors investigated the relationships among elements as well as age-related changes of elements in both the xiphoid process and costal cartilage and found that there was an age-dependent decrease of S in the costal cartilage, but not in the xiphoid process. With regard to the relationships among elements, the common finding that there were significant direct correlations both between Ca and P contents and between Ca and Mg contents, whereas there were significant inverse correlations both between Ca and S contents and between P and S contents obtained in the xiphoid process and costal cartilage.

MATERIALS AND METHODS Sampling of Cartilages Cadavers were treated by injection of a mixture of 36% ethanol, 13% glycerin, 6% phenol, and 6% formalin through the femoral artery (14). After the ordinary dissection by medical students was finished, the xiphoid processes, bilateral the fourth costal cartilages, pubic symphyses, medial menisci, articular disks of the temporomandibular joints, and intervertebral disks between the sixth and seventh cervical vertebrae were resected from 26 subjects and washed thoroughly with distilled water.

Determination of Elements The samples of cartilages were dried at 80°C for 16 h. After 1 mL nitric acid was added, the mixtures were heated at 100°C for 2 h. After the addition of 0.5 mL perchloric acid, they were heated at 100°C for an additional 2 h. The samples were adjusted to a volume of 10 mL by adding ultrapure water and filtering through filter paper (No. 7; Toyo Roshi Co., Osaka, Japan). The resulting filtrates were analyzed with an inductively coupled plasma–atomic emission spectrometer (ICPS-1000III; Shimadzu Co., Kyoto, Japan) (15). The conditions were 1.2 kW of power from a radiofrequency generator, a plasma argon flow rate of 1.2 L/min, a cooling gas flow of 14 L/min, a carrier gas flow of 1.0 L/min, an entrance slit of 20 µm, an exit slit of 30 µm, a height of observation of 15 mm, and an integration time lapse of 5 s. The amount of element was expressed on a dry-weight basis.

Statistical Analysis Statistical analyses were performed using the GraphPad Prism Version 2.0 (GraphPad Software Inc., San Diego, CA, USA). Pearson’s correlation was Biological Trace Element Research

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Elements in the Cartilages

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Fig. 1. Age-related changes of the S content in the xiphoid process (A) and costal cartilage (B).

used to investigate between parameters. A p-value < 0.05 was considered to be significant. Data were expressed as the mean ± standard deviation.

RESULTS The subjects consisted of 17 men and 9 women, ranging in age from 52 to 96 yr (average age = 76.2 ± 11.8 yr).

Age-Related Changes of Elements in the Xiphoid Processes and Costal Cartilages Figure 1 shows age-related changes of the S content in the xiphoid processes (Fig. 1A) and costal cartilages (Fig. 1B). The correlation coefficients between age and S content were estimated to be – 0.007 (p = 0.970) in the xiphoid processes and –0.477 (p = 0.0006) in the costal cartilages. There was an extremely significant inverse correlation between age and S Biological Trace Element Research

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Fig. 2. Relationships between Ca and P contents in the xiphoid process (A) and costal cartilage (B). The numbers of the xiphoid process and costal cartilage were 26 and 52, respectively.

content in the costal cartilages, but not in the xiphoid processes. The correlation coefficients between age and element contents in the xiphoid processes were estimated to be 0.097 (p = 0.639) for Ca, 0.087 (p = 0.673) for P, 0.192 (p = 0.348) for Mg, 0.281 (p = 0.165) for Na, –0.041 (p = 0.842) for Zn, –0.092 (p = 0.656) for Fe, and –0.132 (p = 0.519) for Si. In the costal cartilages, the correlation coefficients between age and element contents were estimated to be 0.184 (p = 0.211) for Ca, 0.158 (p = 0.283) for P, 0.131 (p = 0.374) for Mg, –0.115 (p = 0.436) for Na, 0.193 (p = 0.190) for Zn, 0.185 (p = 0.207) for Fe, and –0.118 (p = 0.426) for Si. Therefore, no significant correlations were found between age and content of elements, such as Ca, P, Mg, Na, Zn, Fe, and Si in the xiphoid processes and costal cartilages.

Relationships Between Ca and the Other Element Contents Figure 2 shows the relationships between Ca and P contents in the xiphoid processes (Fig. 2A) and costal cartilages (Fig. 2B). The correlation Biological Trace Element Research

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Fig. 3. Relationships between Ca and S contents in the xiphoid process (A) and costal cartilage (B).

coefficients between them were estimated to be 0.996 (p < 0.0001) in the xiphoid processes and 0.939 (p < 0.0001) in the costal cartilages, indicating that there were extremely significant direct correlations in the two cartilages. Figure 3 shows the relationships between Ca and S contents in the xiphoid processes (Fig. 3A) and costal cartilages (Fig. 3B). The correlation coefficients between them were estimated to be –0.547 (p = 0.004) in the xiphoid processes and –0.493 (p = 0.0004) in the costal cartilages. There was a very significant inverse correlation between them in the xiphoid processes, whereas there was an extremely significant inverse correlation between them in the costal cartilages. The relationships between Ca and Mg contents in the xiphoid processes and costal cartilages are shown in Fig. 4. The correlation coefficients between them were estimated to be 0.404 (p = 0.045) in the xiphoid processes and 0.537 (p < 0.0001) in the costal cartilages. There was a significant direct correlation between Ca and Mg contents in the xiphoid processes, whereas there was an extremely significant direct correlation in the costal cartilages. Likewise, significant direct correlations were found Biological Trace Element Research

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Fig. 4. Relationships between Ca and Mg contents in the xiphoid process (A) and costal cartilage (B).

between Ca and either Na or Zn contents in the xiphoid processes, whereas significant direct correlations were found between Ca and either Fe or Si contents in the costal cartilages. However, no significant correlations were found between Ca and either Fe or Si contents in the xiphoid processes, whereas no significant correlations were found between Ca and either Na or Zn contents in the costal cartilages (see Tables 1 and 2).

Relationships Between P and the Other Element Contents Figure 5 shows the relationships between P and S contents in the xiphoid processes (Fig. 5A) and costal cartilages (Fig. 5B). The correlation coefficients between them were estimated to be –0.583 (p = 0.002) in the xiphoid processes and –0.439 (p = 0.002) in the costal cartilages, indicating that there were very significant inverse correlations. The relationships between P and Mg contents in the xiphoid processes and costal cartilages are shown in Fig. 6. The correlation coefficients between them were estimated to be 0.380 (p = 0.061) in the xiphoid Biological Trace Element Research

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Table 1 Relationships Among Elements in the Xiphoid Processes

Note: p-Values are indicated in the parentheses.

Table 2 Relationships Among Elements in the Costal Cartilages


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Fig. 5. Relationships between P and S contents in the xiphoid process (A) and costal cartilage (B).

processes and 0.632 (p < 0.0001) in the costal cartilages. Although there was no significant correlation between P and Mg contents in the xiphoid processes, there was an extremely significant direct correlation in the costal cartilages. As shown in Table 1, significant direct correlations were found between P and either Na or Zn contents in the xiphoid processes, but not between P and either Fe or Si contents. Likewise, significant direct correlations were found between P and either Fe or Si contents in the costal cartilages, but not between P and either Na or Zn contents.

Relationships Between S and the Other Element Contents A significant inverse correlation was found between S and Zn contents in the xiphoid processes, but not between the contents of S and elements, such as Mg, Na, Fe, and Si. On the other hand, no significant correlations were found between the contents of S and elements, such as Mg, Na, Zn, Fe, and Si, in the costal cartilages. Biological Trace Element Research

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Fig. 6. Relationships between P and Mg contents in the xiphoid process (A) and costal cartilage (B).

Relationships Between Mg and the Other Element Contents A significant inverse correlation was found between Mg and Fe contents in the xiphoid processes, but not between the contents of Mg and elements, such as Na, Zn, and Si (see Table 1). In the costal cartilages, no significant correlations were found between the contents of Mg and elements, such as Na, Zn, Fe, and Si (see Table 2). As shown in Table 1, with regard to the xiphoid process, no significant correlations were found between the contents of Na and elements, such as Zn, Fe, and Si, between Zn and either Fe or Si contents, and between Fe and Si contents. In the costal cartilages, a significant direct correlation was found between Zn and Fe contents, whereas an extremely significant direct correlation was found between Fe and Si contents (see Table 2). However, no significant correlations were found between the contents of Na and elements, such as Zn, Fe, and Si, and between Zn and Si contents. Biological Trace Element Research

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Furuta et al. Table 3 Relationships Among Elements in the Pubic Symphyses


Relationships Among Element Contents in the Pubic Symphyses, Medial Menisci, Articular Disks of the Temporomandibular Joints, and Intervertebral Disks Tables 3–6 list the relationships among element contents in the pubic symphyses (see Table 3), medial menisci (see Table 4), articular disks of the temporomandibular joints (see Table 5), and intervertebral disks between the sixth and seventh cervical vertebrae (see Table 6). Table 7 summarizes cartilages with significant correlations among the element contents.

DISCUSSION The present study revealed the common finding that there were significant direct correlations both between Ca and P contents and between Ca and Mg contents, whereas there were significant inverse correlations both between Ca and S contents and between P and S contents obtained in the xiphoid processes and costal cartilages. There are many reports (6–13) on calcification or ossification of cartilages. The hyaline cartilage and fibrocartilage are composed mainly of collagen fibers and proteoglycans. It is well known that ossification occurs in Biological Trace Element Research

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Table 4 Relationships Among Elements in the Left Medial Menisci


the xiphoid process in old age (16), whereas calcification occurs in the costal cartilage. Weiss et al. (13) investigated whether different types of cartilage, such as hyaline cartilage, fibrocartilage, and elastic cartilage in the same organism showed any difference during the aging process and revealed that in spite of the apparent biological diversity of the cartilages, the different types of the cartilages underwent a similar pattern of age-related changes. Regarding S in the cartilages, S appeared to decrease in both the articular disk of the temporomandibular joint (4) and trachea (5) with aging, whereas it appeared to increase in the intervertebral disk (1), pubic symphysis (2), and meniscus (3). Dearden et al. (6) investigated age-related changes of the human costal cartilage using the histochemical technique and reported that chondroitin sulfate decreased in the costal cartilage with increasing age, whereas keratan sulfate presumably increased. In the present study, S decreased gradually in the costal cartilage with aging, but not in the xiphoid process. The xiphoid process and costal cartilage belong to hyaline cartilage, whereas the pubic symphysis, meniscus, articular disk of the temporomandibular joint, and intervertebral disk belong to fibrocartilage. As for the fibrocartilages, S appeared to increase with aging, except for the articular disk of the temporomandibular joint. In contrast, S appeared to decrease with aging in hyaline cartilages of the costal cartilage and trachea, but not in the xiphoid process. S contains in both proteoglycans and collagen fibers. Biological Trace Element Research

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Table 5 Relationships Among Elements in the Articular Disks of the Temporomandibular Joints


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Table 6 Relationships Among Elements in the Intervertebral Disks Between Sixth and Seventh Cervical Vertebrae


Table 7 Cartilages with Significant Correlation Among Elements

Note: X, xiphoid process; C, costal cartilage; P, pubic symphysis; M, left medial meniscus; T, articular disk of the temporomandibular joint; I, intervertebral disk.

The authors (17–19) previously investigated the tendons, being composed mainly of collagen fibers. With regard to the relationships among element contents, the common finding that a significant direct correlation was found between S and P contents was obtained in the Achilles’ tendon and insertion’s tendons of the iliopsoas and biceps brachii muscles. The present study revealed that there were significant inverse correlations between S Biological Trace Element Research

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and P contents in the costal cartilage, xiphoid process, and pubic symphysis. Therefore, P increased in proportion to S in the three tendons, whereas P decreased in inverse proportion to S in the three cartilages. These findings suggested that there was no common significant correlation among element contents between the examined cartilages and tendons. The authors (20–22) previously investigated the relationships among element contents in the arteries and found that there were significant direct correlations among the contents of Ca, P, and Mg, whereas there were significant inverse correlations between the content of S and elements, such as Ca, P, and Mg, with some exceptions. In at least the three cartilages, there were significant direct correlations between Ca and either P or Mg contents and there were also significant inverse correlations between the contents of S and elements, such as Ca, P, and Mg (see Table 7). However, there were no significant direct correlations between P and Mg contents in the cartilages, except for the costal cartilage. Excepting the relationship between P and Mg contents, the relationships among the contents of Ca, P, S, and Mg in the cartilages were similar to those in the arteries.

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