Open Access
Open Peer Review

This article has Open Peer Review reports available.

How does Open Peer Review work?

Geographical distribution, a risk factor for the incidence of lupus nephritis in China

  • Qingjun Pan1,
  • Yaning Li1,
  • Ling Ye1,
  • Zhenzhen Deng1,
  • Lu Li1,
  • Yongmin Feng1,
  • Weijing Liu1 and
  • Huafeng Liu1Email author
BMC Nephrology201415:67

DOI: 10.1186/1471-2369-15-67

Received: 17 September 2013

Accepted: 26 April 2014

Published: 1 May 2014

Abstract

Background

Geographical variation in lupus nephritis epidemiology may indicate important environmental factors contributions to the etiology of lupus nephritis. This paper first describes the epidemiology of biopsy-proven lupus nephritis in China by performing a systematic literature review and the possible social-environmental influential factors.

Methods

The keywords “lupus nephritis”, “renal biopsy” and “systemic lupus erythematous” were searched in the three largest Chinese electronic databases and Medline/PubMed. The data of the patients with biopsy-proven lupus nephritis were extracted. The possible environmental influential factors including the population density, ethnic group populations, the ratio of females to males, the average sunshine per year, annual average temperature and annual relative humidity, in different regions of China were analyzed.

Results

Forty-one study centers with 34574 renal disease patients, and 3699 lupus nephritis patients met the inclusion criteria. Lupus nephritis accounts for 2.37% to 25% of all renal disease and 27.2% to 80.65% of renal disease associated with secondary glomerular diseases. The male-to-female ratio is approximately 1:5 in lupus nephritis patients. The included period is predominantly from 1995 to 2010. The proportion ratio of biopsy-proven lupus nephritis in all renal disease or in secondary glomerular disease significantly increased with decreasing latitude from the north to the south part of China. The population is predominantly Han Chinese.

Conclusions

Geographical distribution appears to be a risk factor for the incidence of biopsy-proven LN in China.

Keywords

Biopsy Lupus nephritis Geographical distribution China

Background

Environmental and genetic factors interact to result in the development of systemic lupus erythematous (SLE) [1]. Many epidemiologic studies of SLE have been undertaken worldwide [2, 3] and have detailed worldwide SLE epidemiology, considering the effects of gender, race, and age on presentation and mortality [4, 5].

Renal involvement is common in SLE patients, although accurate current data and systematic investigation of the epidemiology of lupus nephritis (LN) worldwide are largely lacking [6]. The epidemiology of LN based on a selected population and the diagnostic criteria for defining SLE was reported [7]. The LN cumulative incidence is lower in Caucasians (14%) with SLE compared with Asians (55%), African lineages (51%) and Hispanics (43%) with SLE [8, 9]. LN is associated with more severe renal involvement in the patients from African lineage, Hispanics and Asian populations [914]. Also, LN is more likely to be associated with severe nephritis in children and less likely to be associated with severe neuritis in the elderly [15].

These reviews included very few studies conducted in China. There is no systematic investigation of the epidemiology of LN in China. Reports of the incidence of biopsy-proven LN in different geographical regions of China have yielded different results, possibly because the vast territory and a huge population of China results in marked differences in environmental and genetic risk factors for LN. Research papers published in Chinese or other languages are yet to be reviewed to determine the epidemiology of biopsy-proven LN in China.

In this study, we examined the association between geographic distribution and the epidemiology of biopsy-proven LN in China by summarizing 41 studies on LN disease published in different parts of China. We found that LN may be more prevalent in southern China.

Methods

Search strategy: “Lupus nephritis”, “renal biopsy” and “systemic lupus erythematous” were the key words searched in the three largest Chinese electronic databases including the China National Knowledge Infrastructure (CNKI, http://www.cnki.net, inception 1994), Wan Fang (http://www.wanfangdata.com.cn, inception 1982), and Vi Pu (http://www.cqvip.com, inception 1989) The identical keywords with “Chinese” and “China” were searched in the database of Medline/PubMed for papers published from the inception of the databases to July 2013. The data of the patients with lupus nephritis diagnosed by renal biopsy were extracted and analyzed. The geographical distributions of the cities in which the study centers were located were found with Google Maps. We reviewed each paper with inclusion and exclusion criteria.

Inclusion and exclusion criteria: The inclusion criteria for the analyzed papers are as follows: (1) the location of the study centers are in mainland China; (2) the number of patients with biopsy-proven renal diseases was more than 100 cases in each paper; (3) the define of LN was by renal biopsy. (4) The diagnostic criteria for the studies are as follows: the classification of each patient's pathological histological type of renal disease was according to the WHO criteria for the histological classification of glomerular defined in 1982 [16] and revised in 1995 [17] and the criteria of the ISN/RPS. The exclusion criteria for this study are papers that do not meet any items of (1), (2), (3) and (4).

Data Analysis: The characteristics of the analyzed studies included the geographical distribution of the study centers, the research period, and the ratio of the number of females to males for all of the renal biopsies or the LN group, if provided. Pearson's correlation coefficients were calculated to assess the linear association between the proportions of the biopsy-proven LN in all renal diseases or in secondary glomerular diseases (SGD) and the geographical distribution of the study centers. The calculations were performed with SPSS (14.0) software, and statistical significance was established at p < 0.05.

The possible influential factors: To investigate the possible factors that are influential on geographical variation in the epidemiology of biopsy-proven lupus nephritis in China, we investigated the population density, ethnic group populations, the ratio of females to males, the average sunshine per year, annual average trmperature and annual relative humidity in different regions of China.

Results

The characteristics of the study centers included in the analyses

Our literature searches yielded 41 studies that met the study validation criteria (Table 1) [1858], which all originate from the Chinese databases. All of the selected studies were retrospective and included 34574 biopsy-proven renal disease patients and 3699 biopsy-proven LN patients. The World Health Organization 1995 Classification System (issued in 1982) is the most commonly used criteria for patients who had a renal biopsy. The study centers were normally distributed in China (Figure 1A) and most of the study period was from 1995 to 2010 (Figure 1B).
Table 1

Basic information of the 41 studies which met the study validation criteria

No

Ref. (First author,Ref, Year)

Distribution (°)

Biopsy-proven LN

All biopsy-proven renal diseases

Lat.

Long.

Cases

(LN/all renal diseases) ×100%

(LN/SGD) ×100%

Sex (F/M Ratio)

Cases

Begin

End

Sex (F/M Ratio)

Age (average ± S.D, range)

1

Xu YZ [18] 2009

21.11

110.30

322

19.77

65.04

 

1627

1999

2007

1.01

30.7 ± 15.1

2

Luo Q [19] 2008

22.35

113.46

76

12.40

60.80

 

615

2000

2007

1.00

F (33.1 ± 7.8), M (33.56 ± 13.3)

3

Mo WG [20] 2004

22.47

108.20

309

20.61

80.26

5.44

1499

1999

2004

1.07

30.52

4

Zhong HB [21] 2007

26.02

117.36

95

10.41

53.07

 

913

1993

2006

0.70

30.12 ± 15.37

5

Chen JY [22] 2008

26.02

119.18

31

11.52

62.00

 

269

1998

2007

0.78

11-68

6

Zhu CL [23] 2003

26.34

106.42

25

25.00

80.65

 

100

1999

2002

1.70

40.7 ± 28.3

7

Li SR [24] 2004

28.00

119.31

12

10.62

46.15

 

113

1996

2004

1.05

36, 14-73

8

Ke YJ [25] 2004

28.00

121.20

20

17.70

  

113

2000

2002

0.61

32.8

9

Xiang XQ [26] 2005

28.12

113.00

87

7.18

  

1211

1989

2004

 

35.16 (1989-1997)

35.65 (2000-2004)

10

Sun T [27] 2006

29.33

106.32

46

9.41

54.76

4.75

489

2004

2005

1.39

32 ± 16

11

Shi XD [28] 2003

30.15

119.14

82

12.26

55.78

 

669

1992

2001

1.42

9-79

12

Xu YC [29] 2005

30.39

104.05

15

11.00

53.57

 

140

2000

2003

0.94

40.5, 13-70

13

Liu K [30] 2007

31.12

121.29

21

19.63

63.64

 

107

2003

2005

1.55

32.9

14

Yu JP [31] 2000

31.12

121.29

17

9.60

  

177

1994

1999

0.86

34.47

15

Chen HP [32] 2000

31.20

118.50

1319

12.45

74.14

 

10594

1979

2000

0.97

31.4 ± 13

16

Peng YP [33] 2005

31.51

114.52

19

10.80

67.40

 

176

2000

2004

1.29

38, 13-74

17

Wang T [34] 2010

32.03

118.50

44

5.47

34.92

 

805

2003

2008

0.98

36.12 ± 16.08

18

Fan YL [35] 1995

33.96

116.23

6

5.66

  

106

1989

1992

0.58

32, 13-60

19

Du JL [36] 2006

34.15

110.54

220

14.27

53.14

14.7

1542

2000

2004

0.65

33.5 ± 11.8 (LN)

20

Shi J [37] 2010

34.15

110.54

6

2.37

11.76

 

253

2005

2008

0.85

32 ± 16

21

Wang HX [38] 2007

34.16

117.11

40

11.36

41.70

 

352

1998

2007

1.10

38 ± 9.5

22

Li SK [39] 2009

34.16

117.11

59

7.94

38.82

4.36

743

2005

2008

0.79

30.09 ± 14.19

23

Wang YT [40] 2010

34.44

113.53

38

4.13

27.74

 

919

1996

2008

0.81

33.1 ± 14.1, 16-72

24

Zhao ZZ [41] 2005

34.44

113.42

60

14.56

54.55

 

412

2001

2003

0.98

6-69

25

Li XY [42] 2007

34.44

114.51

9

6.25

28.10

 

144

1999

2004

1.18

9-72

26

Zhou SY [43] 2008

36.03

103.49

49

4.08

50.00

 

1202

1994

2006

0.94

31.54

27

Zheng CX [44] 2009

36.63

114.47

33

7.04

31.43

 

469

2000

2008

0.85

34.6, 9-78

28

Huo J [45] 2007

37.51

112.34

72

5.62

27.20

 

1281

1993

2006

0.77

31.6 ± 13.3, 6-74

29

Wang YM [46] 2010

38.03

115.28

14

5.22

26.92

 

268

2004

2009

0.97

35 ± 18, 13-76

30

Zhao CX [47] 2009

38.03

116.83

6

3.16

20.00

 

190

2004

2006

0.92

30.3, 11-67

31

Ding XG [48] 2008

39.36

118.11

21

5.80

37.49

 

362

2005

2007

0.88

34.3 ± 8.2, 11-70

32

Zhang YP [49] 2001

39.54

116.28

142

7.27

37.10

4.46

1954

1987

1999

0.50

33.2 ± 13, 15–73

33

Wang WX [50] 1996

39.54

116.28

13

12.50

38.24

 

104

1989

1994

0.51

13-70

34

Liu WX [51] 2008

39.54

116.28

11

11.00

50.00

 

100

2002

2008

0.82

36.2 ± 14.3, 6-65

35

Hou XY [52] 2009

40.48

111.41

10

4.61

71.43

 

217

2004

2009

0.75

31.8 ± 10.6, 9-70

36

Wang CH [53] 2009

40.48

116.21

40

15.27

48.78

 

262

2005

2008

0.76

37.82 ± 15.51, 12-74

37

Li YQ [54] 2006

41.48

123.24

91

7.03

48.37

7.5

1295

1997

2004

0.77

3.62 ± 8.53, 8-76

38

Feng W [55] 2008

43.46

87.36

87

5.80

34.25

 

1500

1993

2007

0.97

31.4 ± 13, 9-70

39

Yue H [56] 2006

43.46

87.36

12

5.05

41.26

 

237

1999

2005

0.85

35.6 ± 14, 7-74

40

Wang LY [57] 2005

43.55

125.19

53

10.60

43.09

 

500

1984

2004

0.66

39.8 ± 3, 7-74

41

Jiang GT [58] 2008

45.45

126.41

61

11.19

64.20

5.8

545

2003

2005

1.27

1.7 ± 12.6, 8-64

Abbreviation: latitude (Lat.), Longitude (Long.); Femal (F), Male (M), Referance (Ref.), Number (No.).

https://static-content.springer.com/image/art%3A10.1186%2F1471-2369-15-67/MediaObjects/12882_2013_Article_760_Fig1_HTML.jpg
Figure 1

The characteristics of the study centers included in the analyses. The distribution of the studies in China (A), the study period, from the beginning to the end, for all renal diseases (B), the ratio of the number of females to males in all cases of renal disease (C) and the ratio of the number of females to males in LN disease (D).

Based on the forty-one studies, LN was the most common SGD found by percutaneous kidney biopsy and accounted for 2.37% to 25% of all biopsy-proven renal diseases and 27.2% to 80.65% of renal disease biopsies performed for secondary causes of glomerular disease.

The ratio of male-to-female in the biopsy-proven LN patients was approximately 1:5 based on the provided data (Figure 1D) [20, 27, 36, 49, 54, 58]. and approximately 1:1 in all biopsy-proven renal diseases (Figure 1C) [1858].

The correlation between the geographical distribution and the proportion of biopsy-proven LN

The proportion of biopsy-proven LN in all biopsy-proven renal diseases (r = 0.524; P < 0.001) (Figure 2A) and in secondary glomerular diseases (SGD) (r = 0.460; P < 0.001) (Figure 2B) significantly increased in response to the decreasing geographic latitude from the northern part to the southern part of China, but there was no significant correlation with the change in the geographic longitude (all P > 0.05) (Figure 2C, 2D).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2369-15-67/MediaObjects/12882_2013_Article_760_Fig2_HTML.jpg
Figure 2

The correlation between the geographical distribution and the proportion of biopsy-proven LN. The incidence of LN in all renal diseases was correlated with the geographic latitude (A), the incidence of LN in secondary glomerular diseases (SGD) correlated with geographic longitude (B), the incidence of LN in all renal diseases correlated with the geographic latitude (C) and the incidence of LN in secondary glomerular diseases (SGD) with the geographic longitude (D).

The possible influential factors

For the 41 studies, the population density was 400-700 people per Km2 (Figure 3A) in 2000, and the population is predominantly Han Chinese (Figure 3B). Figure 3C showed that there was no significant correlation between the geographical latitude and the ratio of female to male (extracted from China 2000 census) in the population in the southern and northern latitudes of China. In China, the annual sunshine duration ranges from less than 1100 hours in parts of Sichuan and Chongqing to over 3400 hours in northwestern Qinghai. The seasonal patterns in sunshine vary considerably by region, but overall, the north and the Tibetan Plateau are sunnier than the south of the country (Figure 3D). But interestingly, for the annual average temperature and annual relative humidity reported by China Meterological Administration, its guadually increased from the northern to southern latitudes of China, which maybe possible influential factors on the epidemiology of biopsy-proven LN in China (Figure 3E, 3F).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2369-15-67/MediaObjects/12882_2013_Article_760_Fig3_HTML.jpg
Figure 3

The possible influential factors. Population density of China (A); The distribution of Chinese ethnic groups (B); Ratio of females to males in different regions of China (C); Average sunshine per year in different regions of China (D); Annual average temperature (E); Annual relative humidity of China (F).

Discussion

This study is the first to perform a systematic review of the literature to investigate the epidemiology of biopsy-proven lupus nephritis in China. The results showed that geographical distribution appears to be a risk factor for the incidence of biopsy-proven LN in China. The proportion of biopsy-proven LN in all biopsy-proven renal diseases and in the secondary glomerular diseases significantly increased with the decreasing geographic latitude from the northern to the southern part of China, but there was no significant correlation with the change of geographic longitude. The lack of difference in longitudes may be because most studies located in a particular longitude band.

A limited amount of data was available regarding the influence of gender, with only seven studies [20, 27, 36, 39, 54, 58] reporting that the ratio of male-to-female was approximately 1:5 in biopsy-proven LN patients. As was reported, SLE affects women much more frequently than men, but there is considerable regional variation in the ratio of female: male in SLE patients, e.g., in Curaçao (5:3) [59] in Oman (23:1) [60] and in the Philippines (23:1) [61]. One of the major target organs in SLE patients is the kidney, and LN is the most common types of secondary glomerular diseases and frequently seen in females [62, 63].

There are reports of considerable variation in the ratios of female to male according to different geographical area of the world, and we investigated whether the prevalence of biopsy proven-LN is determined by a higher ratio of females to males in populations living in the southern latitude compared to the northern latitude of China. Also, our results showed that there was no significant correlation between the geographic latitude and the ratio of females to males in the populations living in the southern latitude and the northern latitude in China.

We analyzed the environmental and genetic factor interaction in the epidemiology of biopsy proven-LN in China. In the 41 studies, the population density is predominantly 400-700 people per Km2, and the population is Han Chinese. So, the population density and ethnicity may be not decisive factors for the epidemiology of biopsy proven-LN in China. Another important environmental factor is the annual duration of sunshine that ranges from less than 1100 hours in parts of Sichuan and Chongqing to over 3400 hours in northwestern Qinghai. Seasonal sunshine patterns vary considerably by region, but overall, the north and the Tibetan Plateau are sunnier than the south of China, thus the annual sunshine duration may be not decisive factors.

Ultraviolet (UV) radiation, a well-recognized inducement of SLE, but UV radiation-measuring networks are extremely scarce, particularly in China [64]. Also, numerous factors can influence UV radiation, including cloud characteristics, solar zenith angles, total ozone, aerosol pollution and surface albedo. Wei et al [65] reported that the summer UV irradiance has increased significantly from Central China to the northern and western parts of China, especially in Central China near Chongqing, Shanxi, and Hubei provinces; whereas the UV irradiance has decreased significantly in the southern part of China, especially in South China. In July, when UV irradiance is at its maximum and hence when the most serious potential damage may happen, the results indicate an increase in the UV irradiance in Central China and the Yangtze River-Huaihe River valley and a decrease in South China and the eastern part of North China. Thus the influence of ultraviolet radiation on geographical distribution of biopsy-proven LN in China also may be not decisive factors which maybe need to be further investigated.

However, the annual average temperature and annual relative humidity reported by China Meterological Administration, maybe influential factors on the epidemiology of biopsy-proven LN in China. According to a report about the characteristics of seasonal distribution of active SLE and the influences of meteorological factors including temperature and humidity on active SLE in the city of Zhanjiang which is located in the southernmost continent of China, Liu et al found that active SLE has the characteristics of seasonal distribution and is associated with temperature but not related to mean humidity [66].

The majority of LN patients in China receive health care from a doctor near them, and in the 41 studies, most of the doctors are affiliated with hospitals of a medical college or university, well known academic centers or tertiary referral centers for the local regions. A limited number of patients travel to specialist centers for examination and treatment. Beijing (in the northern region), Nanjing (in the central region) and Guangzhou (in the southern region) have among the more renowned academic centers for LN in China. Some patients are not treated for glomerular diseases in a few parts of China, and the criteria for renal biopsy are not identical in different centers. These confounding factors limit the validity of the conclusions to some degree, and further studies are needed to provide an accurate estimate of the absolute risk of geographical distribution related the epidemiology of LN in China. These important clinical questions should be addressed by future prospective studies.

Our study is unique in that it involves primarily a Chinese population. The paper falls within the scope of lupus, and the observations increase the knowledge of the epidemiology of biopsy proven-LN in China.

Conclusions

We summarized the data of the 41 studies of LN disease published in different parts of China and found that geographical distribution appears to be a risk factor for the incidence of biopsy-proven LN in China.

Declarations

Acknowledgements

We would like to thank the support of NSFC (NO.81202346), Natural Science Foundation of Guangdong Province, China (NO.S2012040006216), Zhanjiang Planning Project of Science and Technology (NO.2012C3101028 and 2013B01086), Medical Scientific Research Foundation of Guangdong Province, China (NO.B2012284) and Doctoral Fund of Guangdong Medical College and Affiliated Hospital of Guangdong Medical College to Qingjun Pan.

Authors’ Affiliations

(1)
Institute of Nephrology, Affiliated Hospital of Guangdong Medical College

References

  1. Rahman A, Isenberg DA: Systemic lupus erythematosus. N Engl J Med. 2008, 358 (9): 929-939. 10.1056/NEJMra071297.View ArticlePubMedGoogle Scholar
  2. Vasudevan A, Krishnamurthy AN: Changing worldwide epidemiology of systemic lupus erythematosus. Rheum Dis Clin North Am. 2010, 36 (1): 1-13. 10.1016/j.rdc.2009.12.005.View ArticlePubMedGoogle Scholar
  3. Borchers AT, Naguwa SM, Shoenfeld Y, Gershwin ME: The geoepidemiology of systemic lupus erythematosus. Autoimmun Rev. 2010, 9 (5): 277-287. 10.1016/j.autrev.2009.12.008.View ArticleGoogle Scholar
  4. Tikly M, Navarra SV: Lupus in the developing world–is it any different?. Best Pract Res Clin Rheumatol. 2008, 22 (4): 643-655. 10.1016/j.berh.2008.05.003.View ArticlePubMedGoogle Scholar
  5. Austin HA: Clinical evaluation and monitoring of lupus kidney disease. Lupus. 1998, 7 (9): 618-621. 10.1191/096120398678920749.View ArticlePubMedGoogle Scholar
  6. Patel M, Clarke AM, Bruce IN, Symmons DP: The prevalence and incidence of biopsy-proven lupus nephritis in the UK: evidence of an ethnic gradient. Arthritis Rheum. 2006, 54 (9): 2963-2969. 10.1002/art.22079.View ArticlePubMedGoogle Scholar
  7. Ortega LM, Schultz DR, Lenz O, Pardo V, Contreras GN: Review: Lupus nephritis: pathologic features, epidemiology and a guide to therapeutic decisions. Lupus. 2010, 19 (5): 557-574. 10.1177/0961203309358187.View ArticlePubMedGoogle Scholar
  8. Bastian HM, Roseman JM, McGwin G, Alarcón GS, Friedman AW, Fessler BJ, Baethge BA, Reveille JD, LUMINA Study Group. LUpus in MInority populations: NAture vs nurture: Systemic lupus erythematosus in three ethnic groups. XII. Risk factors for lupus nephritis after diagnosis. Lupus. 2002, 11 (3): 152-160. 10.1191/0961203302lu158oa.View ArticlePubMedGoogle Scholar
  9. Seligman VA, Lum RF, Olson JL, Li H, Criswell LA: Demographic differences in the development of lupus nephritis: a retrospective analysis. Am J Med. 2002, 112 (9): 726-729. 10.1016/S0002-9343(02)01118-X.View ArticlePubMedGoogle Scholar
  10. Kim I, Kim YJ, Kim K, Kang C, Choi CB, Sung YK: Genetic studies of systemic lupus erythematosus in Asia: where are we now?. Genes Immun. 2009, 10 (5): 421-432. 10.1038/gene.2009.24.View ArticlePubMedGoogle Scholar
  11. Adler M, Chambers S, Edwards C, Neild G, Isenberg D: An assessment of renal failure in an SLE cohort with special reference to ethnicity, over a 25-year period. Rheumatology. 2006, 45 (9): 1144-1147. 10.1093/rheumatology/kel039.View ArticlePubMedGoogle Scholar
  12. Contreras G, Lenz O, Pardo V, Borja E, Cely C, Iqbal K, Nahar N, de La Cuesta C, Hurtado A, Fornoni A, Beltran-Garcia L, Asif A, Young L, Diego J, Zachariah M, Smith-Norwood B: Outcomes in African-Americans and Hispanics with Lupus Nephritis. Kidney Int. 2006, 69 (10): 1846-1851. 10.1038/sj.ki.5000243.View ArticlePubMedGoogle Scholar
  13. Korbet SM, Schwartz MM, Evans J, Lewis EJ, Collaborative Study Group: Severe lupus nephritis: racial differences in presentation and outcome. J Am Soc Nephrol. 2007, 18 (1): 244-254. 10.1681/ASN.2006090992.View ArticlePubMedGoogle Scholar
  14. Austin HA, Boumpas DT, Vaughan EM, Balow JE: High-risk features of lupus nephritis: importance of race and clinical and histological factors in 166 patients. Nephrol Dial Transplant. 1995, 10 (9): 1620-1628.PubMedGoogle Scholar
  15. Berden JH: Lupus nephritis. Kidney Int. 1997, 52 (2): 538-558. 10.1038/ki.1997.365.View ArticlePubMedGoogle Scholar
  16. Churg J, Sobin LH: Renal Disease: Classification and Atlas of Glomerular Disease. 1982, Tokyo: Igaku-ShoinGoogle Scholar
  17. Churg J, Bernstein J, Glassock RJ: Renal Disease: Classification and Atlas of Glomerular Diseases. 1995, New York: Igaky-Shoin, 2Google Scholar
  18. Xu YZ, Tan DS, Liu HF, Lin HP, Liang D, Huang ZQ: Clinicopathological analysis on 1672 biopsies of glomerular diseases. J Guangdong Med Coll. 2009, 27: 377-379. (in Chinese)Google Scholar
  19. Luo Q, Xiong ZB, Xiong ZY, Wang Q, Zhang Y, Hou S, et al: Clinicopathological analysis on 615 cases of renal biopsy of adult people. Chin J Integr Tradit West Nephrol. 2008, 9: 531-(in Chinese)Google Scholar
  20. Mo WG, Zeng JJ, Feng ZB, Liao YJ: Analysis of the prevalence and pathological types of 1499 cases of biopsy-proven kidney disease. J Guangxi Med Univ. 2004, 21: 850-853. (in Chinese)Google Scholar
  21. Zhong HB, Huang S, Yu YH, Yang SX, Liao AN, Wang XH: Clinical and pathological features of 913 cases remote mail renal biopsy data. Chin J Integr Trad Wes Nephrol. 2007, 8: 154-156. (in Chinese)Google Scholar
  22. Chen JY, Yuan ZY: Clinicopathological analysis of 269 Renal Biopsies. Mod Med Health. 2008, 24: 2012-2013. (in Chinese)Google Scholar
  23. Zhu CL, Chen YF, Peng HY, Gong Y: Signification of clinicopathological analysis on 100 biopsies of nephritic diseases. Guizhou Med J. 2003, 27: 345-347. (in Chinese)Google Scholar
  24. Li SR, Jiang QH, Chen CS, Hu XM, Shao GJ: Analysis of 113 renal biopsies. Jiangxi Med J. 2004, 39: 197-198. (in Chinese)Google Scholar
  25. Ke YJ, Wu GH, Li YS, Chen YJ, Yang JP, Chen XL, Dai ZY, Gao XF: Clinicopathological analysis of 113 renal biopsies. Chin J Integr Trad Wes Nephrol. 2004, 5: 546-547. (in Chinese)Google Scholar
  26. Xiang XQ, Xia YC, Liu YH, Peng YM, Jiang WL, Li J: Comparative analysis of pathology and clinic on 1211 cases of renal biopsy of adult people. J Cent South Univ Technol. 2005, 30: 733-735. in ChineseGoogle Scholar
  27. Sun T, Zhao HW, Wu XF, Wang DZ, Li L: Clinical pathological analysis of 489 renal biopsies. Chongqing Med J. 2006, 35: 934-937. (in Chinese)Google Scholar
  28. Shi XD, Chen SF, Hu XQ, Fan DY: Pathological analysis of 669 renal biopsies. Zhejiang Clin Med J. 2003, 5: 724-725. (in Chinese)Google Scholar
  29. Xu YC, Yang Q, Dong DD, Li K: Pathological analysis of 140 renal biopsies. Sichuan Med J. 2005, 26: 629-631. (in Chinese)Google Scholar
  30. Liu K, Chen XY: Analysis of 107 renal biopsies. Appl J Gen Pract. 2007, 5: 384-Google Scholar
  31. Yu JP, Yang XY, Cui RL, Yuan WJ: Clinical analysis of 177 percutaneous renal biopsies. Acad J Sec Mil Med univ. 2000, 21: 800-in ChineseGoogle Scholar
  32. Chen HP, Zeng CH, Hu WX, Wang QW, Yu YS, Yao XD, Tang Z, Wang JP, Zhu MY, Zhou H, Liu H, Liu ZH, Li LS: Analysis of 10594 renal biopsies data. Chin J Nephrol Dial Transpl. 2000, 9: 501-509. (in Chinese)Google Scholar
  33. Peng YP, Li J, Liu ZW, Yin ST: Clinicopathological analysis on 176 renal biopsies. Anhui Med J. 2005, 26: 531-532. (in Chinese)Google Scholar
  34. Wang T, Liu DG, Shen JQ, Zhou JD: Analysis on cinical pathological data of 805 cases undergoing renal biopsy in part of Jiangsu province. J Southeast Univ (Med Sci). 2010, 29: 301-305. (in Chinese)Google Scholar
  35. Fan YL, Zhong LM, Lv YX, Wang XL, Meng XH: Clinical application and complications of renal biopsy. Anhui Med J. 1995, 16: 14-(in Chinese)Google Scholar
  36. Du JL, Wang HM, Yu Y, Lian YG, Chen W, Zhang J, Liu YF: Analysis on clinicopathological data of 1542 cases undergoing renal biopsies. Acad J Fourth Mil Med Univ. 2006, 27: 1599-1602. (in Chinese)Google Scholar
  37. Shi J, Liu JH, Tian G: Clinical pathological analysis of 253 renal biopsies. J Pract Med Tech. 2010, 17: 775-776. (in Chinese)Google Scholar
  38. Wang HX, Chen MJ, Wang XY, Wu L: Clinical pathological analysis of 352 renal biopsies. J Chin Phys. 2007, 9: 1699-(in Chinese)Google Scholar
  39. Li SK, Yin ZC, Dai C, Li FC, Zhou SD, Zhang XB, Jin YL: Clinical pathological analysis of 743 renal biopsies. Acta Acad Med Zunyi. 2009, 32: 473-475. (in Chinese)Google Scholar
  40. Wang YT, Xu QY, Guo MH, Zhu TC: Analysis of the prevalence of 919 cases of renal biopsy. Chin J Inte Trad Wes Nephrol. 2010, 11: 232-234. (in Chinese)Google Scholar
  41. Zhao ZZ, Zheng CH, Xiao J, Liu ZS: Clinicopathological analysis on 412 renal biopsies. J Zhengzhou Univ (Med Sci). 2005, 40: 368-369.Google Scholar
  42. Li XY, Xie QK: Clinicopathological analysis on 144 renal biopsies. Chin Med Eng. 2007, 15: 735-737. (in Chinese)Google Scholar
  43. Zhou SY, Tang XP, Zhang PY, Yue XH, Wang YL: Analysis on 1202 renal biopsies in Ultrastructural pathological diagnosis. J Nat Defending Forces Med Southwest Chin. 2008, 29: 60-(in Chinese)Google Scholar
  44. Zheng CX, Duan LP, Hao HY, Xu L, Liu YF: Clinicopathological analysis on 469 renal biopsies in Handan Area. J Clin Nephrol. 2009, 9: 74-75. (in Chinese)Google Scholar
  45. Huo J, Li RS: Characteristics of the prevalence and pathological data of 1281 cases of renal biopsy in Shanxi Province. Chin J Nephrol. 2007, 23: 675-676. (in Chinese)Google Scholar
  46. Wang YM, Liu ZQ: Analysis of 268 clinical cases of renal biopsy. Med Res Educ. 2010, 27: 39-40. (in Chinese)Google Scholar
  47. Zhao CX, Jia LM, Guo TB, Du ST: Clinicopathological analysis on 190 renal biopsies. Mod J Integrated Tradit Chin Western Med. 2009, 18: 3610-(in Chinese)Google Scholar
  48. Ding XG, Li XD, Gao SL, Guo ZJ: Clinicopathological analysis on 362 renal biopsies. Chin J Mod Med. 2008, 18: 1905-1909. (in Chinese)Google Scholar
  49. Zhang YP, Chen XM, Wu D, Chen QS: Analysis of the prevalence and pathological types of 1954 cases of biopsy-proven kidney disease. J Clin Nephrol. 2001, 1: 53-59. (in Chinese)Google Scholar
  50. Wang WX, Zhang L, Zhou W, Shi HB: Clinical pathological analysis of 104 renal biopsies. J Clin Med. 1996, 16: 1-3. (in Chinese)Google Scholar
  51. Liu WX: Analysis on clinicopathological data of 100 cases undergoing renal biopsy. World Health Digest. 2008, 5: 572-574. (in Chinese)Google Scholar
  52. Hou XY, Meng YP, Zhao JR: Clinicopathological analysis on 217 renal biopsies in Nei Menggu area. Chin J Integrated Tradit Wes Nephrol. 2009, 10: 1071-(in Chinese)Google Scholar
  53. Wang CH, Yang LH, Ma F, Liu SY, Zhao JM: Composition analysis of 262 renal biopsies of kidney disease. J Clin Nephrol. 2009, 9: 76-(in Chinese)Google Scholar
  54. Li YQ, Wang Y, Li XL, Yao L, Feng JM, Ma JF, Zhang YX, Wang LN: Analysis of 1259 renal biopsy data in Liaoning area. Chin J Mod Med. 2006, 16: 2830-2833. (in Chinese)Google Scholar
  55. Feng W, Liang LQ, Liu Y, Lie CH: Aziguli: pathological analysis of 1500 renal biopsies. J Clin Nephrolo. 2008, 8 (11): 505-507. (in Chinese)Google Scholar
  56. Yue H, Zhou J, Adila , He W, Qiao LP, Alinuer , Liu J, Sang XH: Analysis on pathologic data and clinical characteristics of renal biopsy in Uyghur and Han nationalities. Xinjiang Med J. 2006, 36: 1-3. (in Chinese)Google Scholar
  57. Wang LY, Liu SJ, Tian Y: Pathological analysis of 500 renal biopsies. Chin J Lab Diagn. 2005, 9: 20-21. (in Chinese)Google Scholar
  58. Jiang GT, Zhang QQ, An HX, Liu SY: Analysis on pathologic data and clinical characteristics of renal biopsy in Heilongjiang. Hei Longjiang Med J. 2008, 32: 423-(in Chinese)Google Scholar
  59. Nossent JC: Systemic lupus erythematosus on the Caribbean island of Curaçao: an epidemiological investigation. Ann Rheum Dis. 1992, 51 (11): 1197-1201. 10.1136/ard.51.11.1197.View ArticlePubMedPubMed CentralGoogle Scholar
  60. Al-Maini MH, El-Ageb EM, Al-Wahaibi SS, Al-Farsi Y, Richens ER: Demographic, autoimmune, and clinical profiles of patients with systemic lupus erythematosus in Oman. Rheumatol In. 2003, 23 (4): 186-191. 10.1007/s00296-003-0303-6.View ArticleGoogle Scholar
  61. Villamin CA, Navarra SV: Clinical manifestations and clinical syndromes of Filipino patients with systemic lupus erythematosus. Mod Rheumatol. 2008, 18 (2): 161-164. 10.3109/s10165-008-0029-0.View ArticlePubMedGoogle Scholar
  62. Haiyan W: Nephrology. 2008, Beijing: People's Medical Publishing House, 1321-1342. ThirdGoogle Scholar
  63. Houssiau FA: Management of lupus nephritis: an update. J Am Soc Nephrol. 2004, 15 (10): 2694-2704. 10.1097/01.ASN.0000140218.77174.0A.View ArticlePubMedGoogle Scholar
  64. Bo H, Yuesi W, Guangren L: Variation characteristics of ultraviolet radiation derived from measurement and reconstruction in Beijing, China. Tellus. 2010, 62B: 100-108.Google Scholar
  65. Ke W, Wen C, Ronghui H: Long-term changes of the ultraviolet radiation in China and its relationship with total ozone and precipitation. Adv Atmos Sci. 2006, 23 (5): 700-710. 10.1007/s00376-006-0700-3.View ArticleGoogle Scholar
  66. Huali Z, Shilhao X, Delhen T, Dong L, Huafeng L: Seasonal distribution of active systemic lupus erythematosus and its correlation with meteorological factors. Clinic. 2011, 66 (6): 1009-1013.View ArticleGoogle Scholar
  67. Pre-publication history

    1. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2369/15/67/prepub

Copyright

© Pan et al.; licensee BioMed Central Ltd. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.

Advertisement