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      Serum levels of PIICP, PIIANP, and PIIBNP are decreased in patients with an endemic osteochondropathy, Kashin-Beck disease

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          Abstract

          Background

          Kashin-Beck disease (KBD) is an endemic, chronic, degenerative osteoarthropathy. KBD is usually diagnosed by using X-ray image and clinical symptoms, lacking of serological biomarkers. The serum level of PIICP, PIIANP, and PIIBNP can specifically reflect the damage of the cartilage. So, in this study, the serum levels of PIICP, PIIANP, and PIIBNP were detected in order to determine whether they can be used as potential biomarkers for the diagnosis of KBD.

          Method

          Using a status survey, the survey sites were selected in the KBD historical endemic areas and non-endemic areas in Jilin and Heilongjiang provinces. All local residents have undergone clinical examination, X-ray examination of the hands and knees, and questionnaire survey. A total of 554 people were surveyed, and 184 residents who are eligible for inclusion criteria were selected as our subjects. Fifty-six cases were diagnosed as KBD and 63 individuals were included as internal control and 65 subjects were included as external control. And blood samples of surveyed subjects were collected, and the serum was separated to detect the levels of PIICP, PIIANP, and PIIBNP by ELISA. Statistical analysis was performed using the SPSS software.

          Results

          There were no statistically significant differences in age and sex among the three groups. The Kruskal-Wallis H test showed that the serum levels of PIICP, PIIANP, and PIIBNP were significantly different among the three groups. Multiple comparisons using Dunnett’s T3 test revealed that serum levels of PIICP, PIIANP, and PIIBNP were significantly lower in KBD patients than in internal and external control. However, there was no significant difference between the internal and external control.

          Conclusions

          The results preliminarily indicated that the levels of PIICP, PIIANP, and PIIBNP in serum could reflect the abnormal synthesis of type II collagen in KBD patients and suggested that these indicators might be used as potential biomarkers for the diagnosis of KBD.

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          Most cited references28

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          Uncoupling of type II collagen synthesis and degradation predicts progression of joint damage in patients with knee osteoarthritis.

          Patrick Garnero, Xavier Ayral, Jean-Charles Rousseau … (2002)
          The hallmark of osteoarthritis (OA) is the loss of articular cartilage. This loss arises from an imbalance between cartilage synthesis and cartilage degradation over a variable period of time. The aims of this study were to investigate the rates of these processes in patients with knee OA using two new molecular markers and to investigate whether the combined use of these markers could predict the progression of joint damage evaluated by both radiography and arthroscopy of the joints during a period of 1 year. Seventy-five patients with medial knee OA (51 women, 24 men; mean +/- SD age 63 +/- 8 years, mean +/- SD disease duration 4.8 +/- 5.2 years) were studied prospectively. At baseline, we measured serum levels of N-propeptide of type IIA procollagen (PIIANP) and urinary excretion of C-terminal crosslinking telopeptide of type II collagen (CTX-II) as markers of type II collagen synthesis and degradation, respectively. Joint space width (JSW) on radiography and medial chondropathy at arthroscopy (assessed using a 100-mm visual analog scale [VAS]) were measured in all patients at baseline and in 52 patients at 1 year. Progression of joint destruction was defined as a decrease of > or =0.5 mm in JSW on radiography and as increased chondropathy (an increase in the VAS score of >8.0 units) between the baseline and 1-year evaluations. At baseline, compared with 58 healthy age- and sex-matched controls, patients with knee OA had decreased serum levels of PIIANP (20 ng/ml versus 29 ng/ml; P < 0.001) and increased urinary excretion of CTX-II (618 ng/mmole creatinine [Cr] versus 367 ng/mmole Cr; P < 0.001). The highest discrimination between OA patients and controls was obtained by combining PIIANP and CTX-II in an uncoupling index (Z score CTX-II - Z score PIIANP), which yielded a mean Z score of 2.9 (P < 0.0001). Increased baseline values in the uncoupling index were associated with greater progression of joint damage evaluated either by changes in JSW (r = -0.46, P = 0.0016) or by VAS score (r = 0.36, P = 0.014). Patients with both low levels of PIIANP (less than or equal to the mean - 1 SD in controls) and high levels of CTX-II (greater than or equal to the mean + 1 SD in controls) had an 8-fold more rapid progression of joint damage than other patients (P = 0.012 and P < 0.0001 as assessed by radiography and arthroscopy, respectively) and had relative risks of progression of 2.9 (95% confidence interval [95% CI] 0.80-11.1) and 9.3 (95% CI 2.2-39) by radiography and arthroscopy, respectively. Patients with knee OA are characterized by an uncoupling of type II collagen synthesis and degradation which can be detected by assays for serum PIIANP and urinary CTX-II. The combination of these two new markers could be useful for identifying knee OA patients at high risk for rapid progression of joint damage.
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            Alternatively spliced type II procollagen mRNAs define distinct populations of cells during vertebral development: differential expression of the amino-propeptide

            N. Morris, M.B. Goldring, L.J. Sandell (1991)
            Type II collagen is a major component of cartilage providing structural integrity to the tissue. Type II procollagen can be expressed in two forms by differential splicing of the primary gene transcript. The two mRNAs either include (type IIA) or exclude (type IIB) an exon (exon 2) encoding the major portion of the amino (NH2)-propeptide (Ryan, M. C., and L. J. Sandell. 1990. J. Biol. Chem. 265:10334-10339). The expression of the two procollagens was examined in order to establish a potential functional significance for the two type II procollagen mRNAs. First, to establish whether the two mRNAs are functional, we showed that both mRNAs can be translated and the proteins secreted into the extracellular environment. Both proteins were identified as type II procollagens. Secondly, to test the hypothesis that differential expression of type II procollagens may be a marker for a distinct population of cells, specific procollagen mRNAs were localized in tissue by in situ hybridization to oligonucleotides spanning the exon junctions. Embryonic vertebral column was chosen as a source of tissue undergoing rapid chondrogenesis, allowing the examination of a variety of cell types related to cartilage. In this issue, each procollagen mRNA had a distinct tissue distribution during chondrogenesis with type IIB expressed in chondrocytes and type IIA expressed in cells surrounding cartilage in prechondrocytes. The morphology of the cells expressing the two collagen types was distinct: the cells expressing type IIA are narrow, elongated, and "fibroblastic" in appearance while the cells expressing type IIB are large and round. The expression of type IIB appears to be correlated with abundant synthesis and accumulation of cartilagenous extracellular matrix. The expression of type IIB is spatially correlated with the high level expression of the cartilage proteoglycan, aggrecan, establishing type IIB procollagen and aggrecan as markers for the chondrocyte phenotype. Transcripts of type II collagen, primarily type IIA, are also expressed in embryonic spinal ganglion. While small amounts of type II collagen have been previously detected in noncartilagenous tissues, the detection of this new form of the collagen in relatively high abundance in embryonic nerve tissue is unique. Taken together, these findings imply a potential functional difference between type IIA and type IIB procollagens and indicate that the removal of exon 2 from the pre-mRNA, and consequently the NH2- propeptide from the collagen molecule, may be an important step in chondrogenesis. In addition, type II procollagen, specifically type IIA, may function in noncartilage tissues, particularly during development.
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              A 5-yr longitudinal study of type IIA collagen synthesis and total type II collagen degradation in patients with knee osteoarthritis--association with disease progression.

              N Charni, J. Kirwan, Munir M. Sharif … (2007)
              The 5-yr longitudinal study tested the hypothesis that serum and urinary markers of type II collagen metabolism would be associated with radiological progression of disease in patients with mild-to-moderate knee osteoarthritis (OA). Synthesis of type IIA collagen and degradation of total type II collagen were assessed in 135 patients with mild-to-moderate knee OA over 5 yrs using serum concentration of the N-propeptide of collagen type IIA (PIIANP) and urinary excretion of crosslinked C-telopeptide (CTX-II), respectively. The markers were measured at baseline, 2, 3 and 5 yrs' follow-up corresponding to X-ray time points. Analysis of variance (ANOVA) was performed to determine longitudinal changes over 5 yrs in the biomarkers in all patients and between progressors and non-progressors. Complete X-ray progression data over 5 yrs, serum PIIANP and urinary CTX-II were available for 84/135 patients. There were 24 progressors and 60 non-progressors. Overall, over the 5-yr study period average PIIANP and CTX-II levels were higher in progressors compared with non-progressors (P < 0.05 for both, ANOVA). The patients with serum PIIANP in the highest quartile of 5-yr levels of PIIANP had a significantly higher risk of progression than the other patients [relative risk (95% CI): 3.2 (1.1-9.2)]. Increased levels of urinary CTX-II were also associated with a higher risk of progression with a relative risk (95% CI) of 3.4 (1.2-9.4) in patients with 5-yr levels above the median. The risk of progression was highest in patients with 5-yr levels of PIIANP in the highest quartile and/or CTX-II in the two highest quartiles with a relative risk (95% CI) of progression, 11.8 (2.5-54). The data presented here suggest that progression of knee OA is associated with alterations of systemic levels of biological markers of type II collagen metabolism. The data also suggest that the combined measurement of serum PIIANP and urinary CTX-II may be useful to identify patients with knee OA at increased risk of disease progression.
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                Author and article information

                Contributors
                Wei Lian: 1287803097@qq.com
                Hui Liu: liuhui@163.com
                Li Yan Sun: 78074451@qq.com
                Yun Qi Liu: liuyunqifbs@163.com
                Si Lu Cui: silubox@163.com
                Yue Wang: 980307865@qq.com
                Quan Quan Song: 1042717737@qq.com
                Qing Deng: dengjohnny@126.com
                Shao Ping Wang: 31599741@qq.com
                Yan Hong Cao: audreycao@yahoo.com
                Xue Ying Zhang: jlsdfbzxy@126.com
                Yuan Yuan Jiang: jiangyuan717@126.com
                Hong Yan Lv: lvhongyan9929@yahoo.com
                Li Bin Duan: jlsdfbdlb@163.com
                Jun Yu:
                ORCID: http://orcid.org/0000-0001-8380-4028
                6yujun@126.com
                Journal
                Journal ID (nlm-ta): J Orthop Surg Res
                Journal ID (iso-abbrev): J Orthop Surg Res
                Title: Journal of Orthopaedic Surgery and Research
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1749-799X
                Publication date (Electronic): 29 May 2018
                Publication date PMC-release: 29 May 2018
                Publication date Collection: 2018
                Volume: 13
                Electronic Location Identifier: 128
                Affiliations
                [1 ]ISNI 0000 0001 2204 9268, GRID grid.410736.7, Institute for Kashin-Beck Disease Control and Prevention, Chinese Center for Disease Control and Prevention, , Harbin Medical University, ; Harbin, China
                [2 ]ISNI 0000 0004 1769 3691, GRID grid.453135.5, Key Laboratory of Etiology and Epidemiology, National Health and Family Planning Commission, ; Harbin, 23618504 China
                [3 ]Jilin Institute of Endemic Disease Prevention Second, Jilin, China
                Author information
                http://orcid.org/0000-0001-8380-4028
                Article
                Publisher ID: 840
                DOI: 10.1186/s13018-018-0840-z
                PMC ID: 5975620
                PubMed ID: 29843748
                SO-VID: 6b749a0d-94bd-4659-90a5-659cd626caa4
                Copyright © © The Author(s). 2018
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 15 December 2017
                Date accepted : 21 May 2018
                Funding
                Funded by: National Natural Science Foundation of China (CN)
                Award ID: 81472931
                Award Recipient :
                Categories
                Subject: Research Article
                Custom metadata
                issue-copyright-statement © The Author(s) 2018

                ScienceOpen disciplines: Surgery
                Keywords: kashin-beck disease,type ii collagen,piicp,piianp,piibnp,biomarkers
                Data availability:
                ScienceOpen disciplines: Surgery
                Keywords: kashin-beck disease, type ii collagen, piicp, piianp, piibnp, biomarkers

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