Chlamydia is a small gram-negative (G−) microorganism that can be dangerous to human and animals. In this study, we conducted a systematic review and meta-analysis of Chlamydia infection in swine in China. From PubMed, ScienceDirect, Chinese Web of knowledge (CNKI), VIP Chinese journal database, and Wanfang database, we collected a total of 72 publications reported in 1985–2020. The prevalence of Chlamydia was 22.48% in China. In the sampling year subgroup, the prevalence after 2011 was the highest (26.14%). In southern China, the prevalence was 30.97%. By contrast, the prevalence in northern China was only 10.79%. Also the difference was significant (p < 0.05). In the provincial level, Hubei had the highest rate of 36.23%. Boars had a higher prevalence (29.47%). The prevalence of Chlamydia detection in pigs with reproductive disorders (21.86%) was higher than that without reproductive disorders. Among the three age groups, finishing pigs (21.43%) had the highest prevalence. The prevalence in large-scale farmed pigs (28.58%) was the highest in the subgroup of feeding methods. The prevalence in farms was 24.29%, which was the highest in the survey areas. The prevalence in spring was the highest with 40.51%. Other methods had the highest prevalence (39.61%) than enzyme-linked immunosorbent assay (ELISA) and indirect hemagglutination assay. The prevalence of Chlamydia psittaci 18.41% was lower than the prevalence of Chlamydia abortus (41.35%). We also analyzed the impact of different climate factor subgroups (rainfall, temperature, and humidity) on the probability of pigs suffering from the disease. The results showed that Chlamydia was widespread in pigs in China. We suggest that we should strengthen the detection of Chlamydia in the semen of breeding pigs and pigs with reproductive disorders, and reasonably control the environment of large-scale pig farms, so as to reduce further infection of Chlamydia in pigs.
Get full access to this article
View all access options for this article.
References
1.
BaiAQ. Serological investigation of Chlamydia suis in some areas of Guangdong. China Anim Livest Vet Med, 2013; 31:37–39. (In Chinese.)
2.
BaiB, LiSF, ZhongWD. Serological investigation of Chlamydia suis in Minhe County, Qinghai Province. Breed Feed, 2018; 17:81–82. (In Chinese.)
3.
BaoTT, WangZR, WuSH, LiangZY, et al.Serological investigation of Chlamydial disease of xiang pig. Guizhou Anim Livest Vet, 2017; 41:40. (In Chinese.)
4.
BarendregtJJ, DoiSA, LeeYY, NormanRE, et al.Meta-analysis of prevalence. J Epidemiol Community Health, 2013; 67:974–978.
5.
BeckerA, Lutz-WohlgrothL, BrugneraE, LuZH, et al.Intensively kept pigs pre-disposed to Chlamydial associated conjunctivitis. J Vet Med A Physiol Pathol Clin Med, 2007; 54:307–313.
6.
BiJL, YangB, GaoLB, YangGS, et al.Serological investigation of Chlamydia suis infection in some areas of Yunnan Province. Prog Anim Med, 2011; 32:134–136. (In Chinese.)
7.
BorelN, PolkinghorneA, PospischilA. A Review on Chlamydial Diseases in Animals: Still a Challenge for Pathologists. Vet Pathol, 2018; 55:374–390.
8.
ChahotaR, OgawaH, OhyaK, YamaguchiT, et al.Involvement of multiple Chlamydia suis genotypes in porcine conjunctivitis. Transbound Emerg Dis, 2017; 65:272–277.
9.
ChenXC, HanQY. Application of Non-Immune Pigs in Epidemiological Surveillance of Large-Scale Pig Farms. Chinese Society of Animal Husbandry and Veterinary Medicine, Society of Livestock Infectious Diseases. Proceedings of the Sixth Congress of the Sixth Council and the Sixth Representative Conference of the Teaching Committee, 2016:335–340. (In Chinese.)
10.
ChenZ, JiW, WangY, YanY, et al.Epidemiology and associations with climatic conditions of Mycoplasma pneumoniae and Chlamydophila pneumoniae infections among Chinese children hospitalized with acute respiratory infections. Ital J Pediatr, 2013; 39:34.
11.
ChenZM, XuZS. Serological Investigation of Chlamydia in Pigs in Zhangzhou City. Fujian Journal of Animal Husbandry and Veterinary Medicine, 2002; 24:10. (In Chinese.)
12.
ConrathsFJ, GeueL, GroschupMH, HänelI, et al.Zoonosen der Nutz- und Wildtiere und ihre Bedeutung in Deutschland. Eine Ubersicht [Zoonoses in working- and wild animals and their significance in Germany. An overview]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz, 2004; 47:633–646.
13.
DengB, GeJ, YangXC, LiKH, et al.Investigation on serological infection of Chlamydia in some large-scale pig farms in Shanghai suburbs in 2015. Shanghai J Anim Livest Vet Med, 2016; 3:22–23. (In Chinese.)
14.
DengHY, WenYP, YangJF, WangQX. Serological antibody monitoring of Chlamydia in swine farms around Fuzhou. The 7th Academic Symposium on Swine Disease in Fujian Province, 2013. (In Chinese.)
15.
EggemannG, WendtM, HoelzleLE, JägerC, et al.Prevalence of Chlamydia infections in breeding sows and their importance in reproductive failure. Dtsch Tierarztl Wochenschr, 2000; 107:3–10.
16.
EnglundS, SegerstadC, ArnlundF, WestergrenE, et al.The occurrence of Chlamydia spp. in pigs with and without clinical disease. BMC Vet Res, 2012; 8:1–6.
17.
EverettKD. Chlamydia and Chlamydiales: More than meets the eye. Vet Microbiol, 2000; 75:109–126
18.
FanWX, YuanXF, LiuWC, LiCS. Serological investigation of Chlamydia swine infection. Chin J Anim Poultry Infect Dis, 1998; 20:49–50. (In Chinese.)
19.
FuWL. Study on Production Efficiency and Influencing Factors of Large Scale Pig Breeding in China. Jiangxi Agricultural University, 2016. (In Chinese.)
20.
GaoSD, ChengSM, ZhouJZ, QiuCQ, et al.Detection of serum antibodies to Chlamydia pigs in some pig farms in Gansu Province. Chin Vet Sci, 2003; 33:28–29. (In Chinese.)
21.
GaoSZ, WeiRS, ShiYN, ShuZ, et al.Serological investigation of swine Chlamydia disease in Gansu Province. Swine Ind Sci, 2001; 13–14. (In Chinese.)
22.
GongQL, LiD, DiaoNC, LiuY, et al.Mink Aleutian disease seroprevalence in China during 1981–2017: A systematic review and meta-analysis. Microb Pathog, 2019; 139:103908.
23.
GuyattGH, OxmanAD, VistGE, KunzR, et al.GRADE: An emerging consensus on rating quality of evidence and strength of recommendations. BMJ, 2008; 336:924–926.
24.
HeCL, ChenZS, XieQ, WangD, et al.Serological investigation of chlamydiosis and its control methods. Ningxia J Agric Forest Sci Technol, 1995; 34–35. (In Chinese.)
25.
HeQG, ChenHC, WuB, WangC, et al.Serological investigation of swine Chlamydia and Brucellosis. Chin Vet Sci Technol, 2000; 30:13–14. (In Chinese.)
26.
HuaBJ. Prevention and control of swine Chlamydia. Shandong J Anim Sci Vet Med, 2018; 39:28–29. (In Chinese.)
27.
HuangSQ, WuXS, LiXH, LinRD, et al.Serological survey of chlamydiasis of swine in large-scale pig farms in Longyan City from 2014 to 2016. Livest Poultry Ind, 2019; 30:12–14. (In Chinese.)
28.
HulinV, OgerS, VorimoreF, AazizR, et al.Host preference and zoonotic potential of Chlamydia psittaci and C. gallinacea in poultry. Pathog Dis, 2015; 73:1–11.
29.
IsazaR, MurrayMJ, VanrompayD, YearyT, et al.Use of PCR testing in diagnosing chlamydiosis. J Avian Med, 2000; 14:122–127.
30.
JiaWY, WeiYM, QianZB. Epidemiological and serological survey of major swine epidemic diseases in Zhangye City. J Anim Sci Vet Med, 2017; 36:73–75 + 78. (In Chinese.)
31.
JiangC, GeDH, FanZC, JiaH. Serological investigation of chlamydiasis of pigs in Huai'an District, Huai'an City, Jiangsu Province. China Swine Ind, 2013; 8:41–42. (In Chinese.)
32.
JiangHH. Serological investigation of toxoplasmosis and chlamydiasis in pigs in Jiangxi Province and genotyping of Toxoplasma gondii from pigs from different localities in China. Chinese Academy of Agricultural Sciences; 2014. (In Chinese.)
33.
JiangPH, YangAB, ChenZM, MaX, et al.Serological investigation and analysis of major swine diseases in Guangdong in 2004. Chin J Vet Drugs, 2006; 40:15–17. (In Chinese.)
34.
JiangTT, YangYS, MengQY, FangYL, et al.Serological investigation report of swine Chlamydia disease by indirect hemagglutination test. Hubei J Anim Vet Sci, 1985; 32–34. (In Chinese.)
35.
JiangWC, XiaoKY, XiangXC. Serological investigation of chlamydiasis infection of cattle and swine in Hunan Province. J Hunan Agr Univ (Nat Sci), 1989; 15:97–101. (In Chinese.)
36.
JinAH, GuBL, WeiXY, FangGM. Serological investigation of swine Chlamydia disease in Shanghai and surrounding areas. Shanghai J Anim Livest Vet Med 2005; 23. (In Chinese.)
37.
JinN, YouX, ZhangZQ, XuH, et al. Serological survey of swine Chlamydia disease. Heilongjiang Anim Sci Vet Med 1999; 24. (In Chinese.)
38.
KieckensE, Van den BroeckL, Van GilsM, Morré S, et al. Co-occurrence of Chlamydia suis DNA and Chlamydia suis specific antibodies in the human eye. Vector Borne Zoonotic Dis, 2018; 18:677–682.
39.
LangLM, WangKL, XiongHD, YouY, et al.Serological investigation of Chlamydia pig infection in Henan Province in 2003. Swine Prod, 2004; 19:29. (In Chinese.)
40.
LiHN, ZhaoXL, JuH, SiQ, et al.Serological investigation of swine Chlamydia disease in Inner Mongolia. Mod Anim Livest, 1999; 20:20–21. (In Chinese.)
41.
LiML. Seroepidemiological survey of Chlamydia disease on some large scale pig farms in Hunan. Hunan J Anim Sci Vet Med, 2005; 36–37. (In Chinese.)
42.
LiX, NiHb, RenWX, JiangJ, et al.Seroprevalence of Toxoplasma gondii in horses: A global systematic review and meta-analysis. Acta Trop, 2020; 201:105222.
43.
LiXH. Serological survey of Chlamydia in some large-scale farms in Qinghai Province. Swine Ind Sci, 2004; 21:55–56. (In Chinese.)
44.
LiYL. Seroepidemiological investigation report on chlamydiasis of swine in Chuxiong Prefecture, Yunnan Province. Contemp Anim Livest, 2014:29–30. (In Chinese.)
45.
LiuBS, LiYB, WangQQ, KongFY, et al.Investigation and diagnosis of swine epidemic in summer in Honghe Prefecture in 2002. Yunnan J Anim Sci Vet Med, 2003:16–17. (In Chinese.)
46.
LiuBS, WangQQ, LiuJS, LiYB. Serological investigation of chlamydiasis of pigs in Honghe Prefecture, Yunnan Province. Chin J Vet Med, 2006; 42:33. (In Chinese.)
47.
LiuCL. Large-scale pig farms should not ignore the prevention and control of Chlamydia. Feed Review 2019; 85. (In Chinese.)
48.
LiuP, WangYY, YanLJ, MaZR. Serological investigation of chlamydiosis in sows in small scale farms. Graziery Vet Sci (Electronic Version), 2019; 4–5. (In Chinese.)
LongbottomD, LivingstoneM. Vaccination against chlamydial infections of man and animals. Vet J, 2006; 171:263–275.
51.
LuoGP, HuTY, ZhangYG, LinML, et al. Investigation on chlamydiasis of swine in Mudanjiang Region. Heilongjiang Anim Sci Vet Med 1998; 25. (In Chinese.)
52.
LuoJ, YangXY, DaiAL, LiXH. Seroepidemiological investigation of Chlamydia disease of sows in large-scale pig farms. Fujian J Anim Livest Vet, 2006; 28:4–5. (In Chinese.)
53.
MaCF, GaoJY, HuJX, LiH, et al.Seral antibody detection of Chlamydia in breeding swine herds in Xinyang of Henan Province. Prog Vet Med, 2016; 37:119–122. (In Chinese.)
54.
MaSL, WangGP, MaLQ. Serological survey of swine Chlamydia disease. Chin Qinghai J Anim Vet Sci, 2001; 31:31. (In Chinese.)
55.
MaYL, XuXP, ZhengWA, WangYX. Serological investigation of toxoplasmosis, cysticercosis and Chlamydia of swine. Yunnan J Anim Sci Vet Med 1990; 22. (In Chinese.)
56.
MeiSL. Development of ondirect enzyme-linked immunosorbent assay for detecting antibody against swine Chlamydia abortus. Huazhong Agricultural University; 2009. (In Chinese.)
57.
NieLB. Seroepidemiological Investigation of Chlamydia of Wild Boar and Neospora of Tibetan Sheep, Raccoon Dog and Donkey Dog. Jilin Agricultural University 2019. (In Chinese.)
58.
PagliaraniS, JohnstonSD, BeagleyKW, DiefH, et al.The occurrence and pathology of chlamydiosis in the male reproductive tract of non-human mammals: A review. Theriogenology, 2020; 154:152–160.
59.
PanQ. Construction, Immune Evaluation and Mechanism of Porcine Chlamydia abortus pmp18n rvcg Vaccine. China Agricultural University, 2015. (In Chinese.)
60.
PanYH. Epidemiology, clinical characteristics, laboratory examination and control measures of swine Chlamydia. Mod Anim Livest Sci Technol, 2019:119–120. (In Chinese.)
61.
PantchevA, StingR, BauerfeindR, TyczkaJ, et al.Detection of all Chlamydophila and Chlamydia spp. of veterinary interest using species-specific real-time PCR assays. Comp Immunol Microbiol Infect Dis, 2010; 33:473–484.
62.
PengGW. Serological investigation of swine Chlamydia. Swine Prod, 2006; 21:46. (In Chinese.)
63.
R Core Team. R Core Team, R: Language and Environment for Statistical Computing, 2018.
64.
ReinholdP, KirschvinkN, TheegartenD, BerndtA. An experimentally induced Chlamydia suis infection in pigs results in severe lung function disorders and pulmonary inflammation. Vet Res, 2008; 39:35.
65.
RenYQ, LuHF, LiangHM, ZhangZJ. Investigation of swine Chlamydia disease in Guangdong province. Chin J Vet Med, 1994; 20:37. (In Chinese.)
RypułaK, KumalaA, Płoneczka-JaneczkoK, DudekK, et al.Impact of Chlamydia suis Infection on Reproductive Disorders in Pig Herds. International Conference on Advances in Veterinary Science Research, 2015.
68.
SachseK, BavoilPM, KaltenboeckB, StephensRS, et al.Emendation of the family Chlamydiaceae: Proposal of a single genus, Chlamydia, to include all currently recognized species. Syst Appl Microbiol, 2015; 38:99–103.
69.
SachseK, GrossmannE, JägerC, DillerR, et al.Detection of Chlamydia suis from clinical specimens: Comparison of PCR, antigen ELISA, and culture. J Microbiol Methods, 2003; 54:233–238.
70.
SachseK, LaroucauK, RiegeK, WehnerS, et al.Evidence for the existence of two new members of the family Chlamydiaceae and proposal of Chlamydia avium sp. nov. and Chlamydia gallinacea sp. nov. Syst Appl Microbiol, 2014; 37:79–88.
71.
SchautteetK, VanrompayD. Chlamydiaceae infections in pig. Vet Res, 2011; 42:29.
72.
ShiXC. The Epidemiological Investigation of Six Pig Contagious Diseases in Tibet Pigs in Linzhi. Northwest A & F University, 2013. (In Chinese.)
73.
SuYX, ZhangSL, WeiHX, TongC. Serological investigation of swine Chlamydia infection in Pingdingshan area. Swine Prod, 2002; 17:45. (In Chinese.)
74.
SunGJ. Investigation and Analysis of Major Epidemic and the Cause to Sow Reproductive Disorder of Large-Scale Pig Farm in Shandong Province. Qingdao Agricultural University, 2011. (In Chinese.)
75.
SunJW, WangM. Serological investigation of chlamydiasis of pigs in Ganxian County, Shaanxi Province. Farm Technol, 2014; 30:313. (In Chinese.)
76.
SuoXF, WangDL, ZhangSH, WangJX, et al.Seroepidemiological survey of Chlamydia disease in large-scale pig farms in Hainan Province. Swine Production, 2005; 20:31–32. (In Chinese.)
77.
TianDY, LiuZX, LiJ, LiJJ, et al.Preliminary investigation on the epidemic situation of Chlamydia abortus in intensive pig farm China. Anim Livest Vet Med, 2012; 39:210–213. (In Chinese.)
78.
VanrompayD, NeromAV, DucatelleR, HaesebrouckF. Evaluation of five immunoassays for detection of Chlamydia psittaci in cloacal and conjunctival specimens from turkeys. J Clin Microbiol, 1994; 32:1470–1474.
79.
WangHZ. Serological investigation of swine chlamydiasis on large-scale pig farm. Mod J Anim Livest Vet Med, 2004; 33:26. (In Chinese.)
80.
WangJC, FuQ, WangJF, TianZX. Serological testing of Chlamydia in the imported breeding animals in Hebei Province. China Anim Health Inspect, 2012a; 29:48–49. (In Chinese.)
81.
WangM. China's pig industry: Summary at the end of 2018 and outlook at the beginning of 2019. Swine Ind Sci, 2019; 36:142–143. (In Chinese.)
82.
WangN. How to conduct a meta-analysis of proportions in R: A comprehensive tutorial. 2018; [Epub ahead of print]; DOI: 10.1314/0/RG.2.2.27199.00161.
83.
WangQQ, LiuBS, LiYB, WangZH, et al.Isolation and identification of pathogens of Chlamydia pig abortion in Honghe Prefecture, Yunnan Province. Chin Vet Sci, 2001; 31:19–20. (In Chinese.)
84.
WangSR, FengXR, MiaoLY. Serological diagnosis and clinical investigation of swine Chlamydia disease. Henan J Anim Livest Vet Med, 1997; 22:18–19. (In Chinese.)
85.
WangWF, ZhouYF. Serological investigation of the Chlamydia infection of mutual help Bamei pig. Swine Prod, 2009; 24:72. (In Chinese.)
86.
WangXQ, GaoY, LiGY, HeXH, et al.Serological investigation of goose chlamydiosis in Qingyuan City, Guangdong Province. China Poult, 2012b; 34:63–64. (In Chinese.)
87.
WangYJ. Study on the Development and Market Strategy of Meat Industry in China. Huazhong Agricultural University, 2006. (In Chinese.)
88.
WeiYM. Serological survey of swine Chlamydia disease in intensive pig farm. Chin J Zoonoses, 2011; 18:116–113. (In Chinese.)
89.
WenFH, HongM, LinQ. Investigation and research on chlamydiasis of pig farms on multiple scales. Fujian J Anim Livest Vet Med, 2007; 29:57–58. (In Chinese.)
90.
WuYX, WuJJ. Antibody detection of Parvovirus, Japanese encephalitis virus, Pseudorabies virus and Chlamydia in swine serum. Sichuan Anim Vet Sci, 1992; 21–22. (In Chinese.)
91.
XianQZ, CaiMF, WangSM, HuangLZ. Serological investigation and control of Chlamydia disease in small and medium-sized pig farms in Guangdong and Guangxi. J Anim Livest Vet Med, 2007; 20–21. (In Chinese.)
92.
XieQ, GaoYL, HeCL, ShiJB, et al.Application of monoclonal antibody in serum diagnosis of animal Chlamydia disease. Chin J Prev Vet Med, 2001; 23:72–73. (In Chinese.)
93.
XuRS, CaiXD, ShenY, WuSH, et al.Serological survey of several zoonoses in pigs. China Anim Health Inspect, 2001; 18:40–41. (In Chinese.)
94.
YanSX. Preparation of Monoclonal Antibody Against Chlamydia abortus and Establishment of Blocking ELISA. Huazhong Agricultural University, 2013. (In Chinese.)
95.
YangF, LiM, LiJ, WangYY, et al.High prevalence and genetic diversity of Chlamydia suis in Zhejiang Province. Anim Livest Vet Med, 2018; 50:51–55. (In Chinese.)
96.
YangXM, XieJ, LinY. Serological diagnosis of swine reproductive disorders. Sichuan Anim Vet Sci, 2003; 30:4–6. (In Chinese.)
97.
YangYS, JiangTT, FangYL, LiGM. Preliminary report on serological investigation of sow infectious reproductive disorder. Hubei J Anim Vet Sci, 1991; 25–29. (In Chinese.)
98.
YaoSX, SongDL, RenXL, HangBL, et al.Serological investigation of porcine Chlamydia disease. Today Anim Livest Vet Med, 2007; 4–6. (In Chinese.)
99.
YeRQ, ZhaiWC, GuWJ. Detection of serum antibody of Chlamydia pig in intensive pig farm. Chin J Vet Sci Technol, 2001a; 31:19–20. (In Chinese.)
100.
YeT. Key points of national animal husbandry work in 2010. Agr Technol Eq, 2010:18–20. (In Chinese.)
101.
YeW, LinQ, WuJH, WangYL, et al.Serological survey of swine Chlamydia disease. Shanghai J Anim Livest Vet Med, 2001b; 50:30. (In Chinese.)
102.
YiQZ, ChenZX, ZhengLF, ZhouGJ. Serological investigation of swine chlamydiosis in Guangxi. Chin J Vet Med, 1994; 20:20. (In Chinese.)
103.
YuHK, WuJZ, WangYH, ShenC. Analysis on the current situation, mode and regional distribution of pig breeding industry in China. China Swine Ind, 2018; 13:23–26. (In Chinese.)
104.
ZhangJN, SongCX, GuWW, WuQH. Serological Survey of Ten Kinds of Infectious Diseases in Mini-Pigs in Tibet. The 9th China-South Africa Laboratory Animal Science and Technology Exchange, 2009. (In Chinese.)
105.
ZhangLC, WangXZ, ZhangMH, LaH, et al.Serological surveillance of livestock Chlamydia disease in Qinghai Province. Chin J Vet Med, 2014a; 50:38–39. (In Chinese.)
106.
ZhangN, ZhuZY, ZhangLY, LiuCS. Development situation and Countermeasures of pig industry in Northeast China. China Feed, 2018; 72–75. (In Chinese.)
107.
ZhangNG, ZhangZL, LiuQL, FanYC. Serological investigation of swine Chlamydia disease in Shanghang County. Fujian J Anim Livest Vet Med, 2005; 27:23. (In Chinese.)
108.
ZhangXP, LiYE, WenQP, LaiXX. Serological investigation of five kinds of pig diseases in Dongguan. Prog Vet Med, 2006; 27:111–112. (In Chinese.)
109.
ZhangXX, LiRC, LiuGH, CongW, et al.High seroprevalence of Chlamydia infection in sows in Hunan Province, subtropical China. Trop Anim Health Prod, 2014b; 46:701–704.
110.
ZhengZY. Serological Investigation of Four Important Diseases in Pigs in Jilin Province. Jilin Agricultural University, 2018. (In Chinese.)
111.
ZhouDN, YangKL, YanSX, LiuZW, et al.Establishment of an indirect ELISA for detecting swine antibodies against Chlamydophila abortu based on recombinant MOMP protein. Chin J Prev Vet Med, 2015; 703–706. (In Chinese.)
112.
ZhouP, LinZY, WangTF, LuoCQ, et al.Seroepidemiological survey of Chlamydia in some pig farms in Longyan, Fujian. Prog Vet Med, 2008; 29:30–35. (In Chinese.)
113.
ZhuYN. Epidemiological investigation of Chlamydia suis in Tianjin. Swine Ind Sci, 2016; 33:82–83. (In Chinese.)
114.
ZhuYQ, WangRB, CaiYQ, HuJC, et al.Seroepidemiological survey of chlamydiasis of swine. Guangdong J Anim Vet Sci, 2007; 32:26–27. (In Chinese.)
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
