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  • Open Access

A report of nine cases and review of the literature of infertile men carrying balanced translocations involving chromosome 5

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  • 1,
  • 1,
  • 1,
  • 1,
  • 1 and
  • 1Email author
Molecular Cytogenetics201811:10

https://doi.org/10.1186/s13039-018-0360-x

  • Received: 14 November 2017
  • Accepted: 16 January 2018
  • Published:

Abstract

Background

Balanced translocations may cause the loss of genetic material at the breakpoints and may result in failure of spermatogenesis. However, carriers of reciprocal translocation may naturally conceive. Genetic counseling of male carriers of translocations remains challenging. This study explores the clinical features of carriers of chromosome 5 translocations, enabling informed genetic counseling of these patients.

Results

Of 82 translocation carriers, 9 (11%) were carriers of a chromosome 5 translocation. One case had azoospermia, while three cases had experienced recurrent spontaneous abortions, two cases had each experienced stillbirth, and three cases produced a phenotypically normal child confirmed by amniocentesis. A literature review identified 106 patients who carried chromosome 5 translocations. The most common chromosome 5 translocation was t(4,5), observed in 13 patients. Breakpoint at 5p15 was observed in 11 patients. All breakpoints at chromosome 5 were associated with gestational infertility.

Conclusion

In genetic counseling, physicians should consider chromosome 5 and its breakpoints. Carriers of chromosome 5 translocations may continue with natural conception or use assisted reproductive technologies, such as preimplantation genetic diagnosis.

Keywords

  • Male infertility
  • Chromosome 5
  • Balanced translocation
  • Breakpoint
  • Genetic counseling

Background

Known chromosomal alterations play a major role in perturbing male fertility [1]. Reciprocal chromosomal translocations are the most common structural rearrangement, with an incidence in infertile males up to ten times higher than in fertile men [2]. Balanced chromosomal translocations may cause the loss of genetic material at breakpoints and may result in failure of spermatogenesis [3]. Individuals affected by such translocations exhibit reproductive problems such as infertility, recurrent pregnancy loss, and malformed offspring [4, 5]. These effects are related to the specific chromosomes and breakpoints involved in the translocation [6, 7]. Some breakpoints can disrupt the structure of an important gene, leading to spermatogenic or maturation disorders, and male infertility [5]. Important genes associated with male infertility are located on chromosome 5. For example, Camk4 (encoding Ca2+/calmodulin-dependent protein kinase IV) is located on chromosome 5q22.1, and is expressed in spermatids and associated with chromatin and nuclear matrix [8]. Disrupted CAMK4 expression may be associated with human male infertility [8]. In addition, the Spink13 gene (encoding serine protease inhibitor, Kazal-type 13), mapped on chromosome 5 at 5q32, was reported to be associated with sperm maturation [9]. The breakpoint of 5p13 was shown to be related to impaired spermatogenesis [10].

However, genetic counseling of male carriers of chromosomal translocations remains challenging. Preimplantation genetic diagnosis (PGD) is recommended for those exhibiting a balanced translocation. Microdissection testicular sperm extraction and in vitro fertilization accompanied by PGD increases the chance of these carriers fathering a healthy child [11, 12]. Clinical characteristics, including spontaneous abortion, do not differ between those couples who accept and those who decline PGD [13]. A systematic review showed there was insufficient evidence that PGD improves the live birth rate in couples with repeated miscarriage and carrying a structural chromosome abnormality [14]. In addition, the live birth rate in patients refused PGD and choosing to conceive naturally was reported to be 37–63% for the first pregnancy, and then a cumulative rate of 65–83% [4]. Natural pregnancy success rates for couples in which the male carries a chromosomal translocation ranged from 30% to 70% [15]. This suggests that continued attempts to conceive naturally are a viable option for successful pregnancy, however, the relationship between clinical features and chromosome structural abnormality warrants further study.

The present study was established to explore the clinical features and translocation breakpoints in carriers of balanced translocations involving chromosome 5. This paper also highlights the importance of genetic counseling for infertile men.

Methods

Patients

Between July 2010 and December 2016, 82 male carriers of chromosomal translocations who were experiencing infertility, or receiving counseling, were recruited from the outpatient’s department at the Center for Reproductive Medicine, the First Hospital of Jilin University, Changchun, China. All patients underwent a thorough physical examination and semen analysis, and were required to complete a detailed questionnaire regarding their smoking habits, marital status, medical history, and working conditions. The study protocol was approved by the Ethics Committee of the First Hospital of Jilin University, and written informed consent was obtained from all participants.

Semen analysis

Semen analysis was performed according to procedures recommended by the World Health Organization guidelines. If no sperm was found, sperm was analyzed by sedimenting semen samples through centrifugation. Patients with oligozoospermia were diagnosed as a sperm count less than 15 × 106/ml in their last three semen samples (taken at intervals of 1–3 weeks). Azoospermia and oligozoospermia were defined as previously described [5]. All analyses were performed at the same laboratory, and all data were accessed from medical records.

Cytogenetic analysis

Cytogenetic analysis was carried out on all patients. Peripheral blood (0.5 mL) was collected in sterile tubes containing 30 U/mL heparin. Lymphocytes were then cultured in appropriate culture medium (Yishengjun; Guangzhou Baidi Biotech, Guangzhou, China) for 72 h, and subsequently treated with 20 μg/mL colcemid for 1 h. G-banding of metaphase chromosomes and karyotype analysis were performed using previously described methods [5]. Twenty metaphases were counted and 6 karyotypes were analyzed per patient. Karyotype nomenclature was described in accordance of ISCN2009. The resolution level of chromosome analysis was 400–550 band levels.

Analysis of the identified translocation breakpoints

A search of translocations identified in chromosome 5 from infertile males was performed using PubMed. The keywords “chromosome / translocation / sperm” and “chromosome / translocation / abortion” were used for the PubMed search. The relationships of translocation breakpoints with male infertility and recurrent pregnancy loss were analyzed. Such searches were performed for a total of 106 carriers of chromosomal 5 translocations. This study included the cases of reciprocal chromosomal translocations involving chromosome 5 in reported papers, and excluded cases without breakpoints, females, newborns, and bone marrow detection involving chromosome 5.

Results

A total of 82 translocation carriers were detected in this study. Of these, nine (11%) were carriers of a chromosome 5 translocation, in which other chromosome abnormality had been excluded. Karyotype results and G-banding karyotypes from these nine patients are respectively summarized in Table 1 and Fig. 1. One case had azoospermia (pregestational infertility), while eight cases had normal semen. For the former, no AZF gene deletion was found. Of the later eight cases, it was evident that their partners were able to conceive, but had a tendency to miscarry (gestational infertility): three cases had experienced recurrent spontaneous abortions, two cases each experienced stillbirths, and three cases produced a phenotypically normal child confirmed by amniocentesis. For the other 73 cases of translocations, we will describe or have published in another study.
Table 1

Karyotypes of chromosome 5 translocation carriers and their clinical features

Infertility causes

Clinical findings

Karyotype

Giemsa banding

Pregestational infertility

Azoospermia

46,XY,t(5;21)(q13;p12)

Figure 1a

Gestational infertility

Normal sperm density; a history of miscarriage, or normal fertility

46,XY,t(4;5)(q31;p15)

Figure 1b

46,XY,t(5;11)(p14;p15)

Figure 1c

46,XY,t(5;13)(q13;q12)

Figure 1d

46,XY,t(5;18)(p13;p11)

Figure 1e

46,XY,t(5;18)(p15;q11.2)

Figure 1f

46,XY,t(5;20)(q13;q12)

Figure 1g

46,XY,t(5;21)(p13;q22)

Figure 1h

46,XY,t(5;22)(p11;p11)

Figure 1i

Fig. 1
Fig. 1

G-banding karyotype of the nine cases identified as possessing chromosome 5 translocations. a: t(5;21), b: t(4;5), c: t(5;11), d:t(5;13), e: t(5;18)(p13;p11), f: t(5;18)(p15;q11.2), g: t(5; 20), h: t(5;21), i: t(5;22)

A literature review was also performed, from which karyotype results, clinical manifestations, and breakpoints on chromosome 5 were collected, as shown in Table 2. A total of 106 karyotypes included chromosome 5 translocations. The most common translocation was t(4;5), observed in 13 patients, followed t(5;8) (N = 11). Chromosomes 4(N = 13), 8(N = 11), 2,3,7,13(N = 7), 1,9,10,12(N = 6), 6, 18(N = 5), 15,20(N = 4),14,16,17(N = 3) and 11,19, X (N = 1) were respectively involved in the balanced translocation with chromosome 5.
Table 2

Breakpoints in chromosome 5 translocation carriers and clinical features

Case

Karyotype

Breakpoints

Clinical findings

Reference

1

t(1;5)

1p32;5q31

Severe oligoasthenoteratozoospermia

Peschka et al., 1999 [27]

2

t(1;5)

1p31.1;5q33.3

Normozoospermia

Brugnon et al., 2006 [28]

3

t(1;5)

1p22;5q11

Malformed/stillborn children

Meza-Espinoza et al., 2008 [29]

4

t(1;5)

1q36.1;5q31

2 miscarriage, PGD and 2 term delivery

Ikuma et al., 2015 [4]

5

t(1;5)

1q41;5q33

Miscarriage and PGD

Kyu Lim et al., 2004 [30]

6

t(1;5)

1qter;5p14

Recurrent miscarriage

Goud et al., 2009 [31]

7

t(2;5)

2p25;5p12

Teratozoospermia, Habitual abortions

Vegetti et al., 2000 [32]

8

t(2;5)

2p21;5p15

Recurrent spontaneous abortion

Gada Saxena et al., 2012 [33]

9

t(2;5)

2p13;5p15

Recurrent fetal wastage

Fryns et al., 1998 [34]

10

t(2;5)

2p11;5q15

Abortion

Templado et al., 1988 [35]

11

t(2;5)

2p11;5q31

Recurrent abortion

Portnoï et al., 1988 [36]

12

t(2;5)

2q12;5q35.3

Recurrent pregnancy loss

Kochhar et al., 2013 [22]

13

t(2;5)

2q13.1;5q35.1

6 miscarriage, PGD and 1 term delivery

Ikuma et al., 2015 [4]

14

t(3;5)

3p27;5p14

4 fetal losses

Adamoli et al., 1986 [37]

15

t(3;5)

3q13;5q35

Repeated abortions

Venkateshwari et al., 2011 [21]

16

t(3;5)

3q26.2;5p15.1

Miscarriage

Sugiura-Ogasawara et al., 2008 [38]

17

t(3;5)

3q27;5p15

Normospermic, A boy 46,XY,t(3;5)pat

Vozdova et al., 2013 [11]

18

t(3;5)

3q28;5p13

Recurrent spontaneous abortion

Gada Saxena et al., 2012 [33]

19

t(3;5)

3q29;5q13

Multiple abortions

Castle et al., 1988 [39]

20

t(3;5)

3q29;5q33.2

PGD

Findikli et al., 2003 [40]

21

t(4;5)

4p15.2;5p12

Normozoospermia

Wiland et al., 2007 [41]

22

t(4;5)

4p15;5q12

Oligozoospermia

Perrin et al., 2010 [42]

23

t(4;5)

4p14;5q13.1

recurrent miscarriage

Pundir et al., 2016 [43]

24

t(4;5)

4q21;5p15

Habitual miscarriage

Li et al., 2012 [23]

25

t(4;5)

4q21;5p15

Recurrent spontaneous abortion

Zhang M et al., 2015 [44]

26

t(4;5)

4q21;5q11.2

Severe oligoasthenoteratozoospermia

Peschka et al., 1999 [27]

27

t(4;5)

4q22;5q35

2 fetal losses

Adamoli et al., 1986 [37]

28

t(4;5)

4q25;5p15.2

4 abortions

Ghazaey et al., 2015 [45]

29

t(4;5)

4q31;5p15

Recurrent spontaneous abortions

Zhang et al., 2011 [46]

30

t(4;5)

4q31;5q13

normozoospermia

Huang et al., 2007 [47]

31

t(4;5)

4q32;5q14

Oligoasthenoteratozoospermia

Dohle et al., 2002 [48]

32

t(4;5)

4q32;5q14

Miscarriage

Dul et al., 2012 [49]

33

t(4;5)

4q35;5p15

Recurrent miscarriages

Dutta et al., 2011 [50]

34

t(5;6)

5p15.3;6q13

recurrent abortion

Kiss et al., 2009 [51]

35

t(5;6)

5p13.3;6q27

Recurrent spontaneous abortion

Gada Saxena et al., 2012 [33]

36

t(5;6)

5q21;6q33

Recurrent fetal wastage

Fryns et al., 1998 [34]

37

t(5;6)

5q33.1;6p11.2

Miscarriage

Sugiura-Ogasawara et al., 2008 [38]

38

t(5;6)

5q35;6p21.3

PGD

Ko et al., 2010 [52]

39

t(5;7)

5p15.2;7p14

Recurrent spontaneous abortion

Gada Saxena et al., 2012 [33]

40

t(5;7)

5p13;7p15

Recurrent pregnancy loss

Kochhar et al., 2013 [22]

41

t(5;7)

5p13;7p15

Spontaneous abortion

Stephenson et al., 2006 [53]

42

t(5;7)

5p11;7q11

8 abortions

Al-Hussain et al., 2000 [54]

43

t(5;7)

5q13;7p15.1

2 miscarriages

Estop et al., 1995 [55]

44

t(5;7)

5q21;7q32

Normozoospermia

Cifuentes et al., 1999 [56]

45

t(5;7)

5q33;7q22

Miscarriage and PGD

Kyu Lim et al., 2004 [30]

46

t(5;8)

5p14;8q22

Asthenozoospermia

Godo et al., 2013 [7]

47

t(5;8)

5q22;8q24.1

Oligoasthenoteratozoospermia

Meschede et al., 1998 [57]

48

t(5;8)

5q22.1;8q23.2

PGD

Ko et al., 2010 [52]

49

t(5;8)

5q23.1;8p23.2

4 miscarriage,1 term delivery

Ikuma et al., 2015 [4]

50

t(5;8)

5q33.3;8q11.21

Recurrent miscarriage

Pundir et al., 2016 [43]

51

t(5;8)

5q33;8q13

Normozoospermia

Blanco et al., 1998 [58]

52

t(5;8)

5q33;8q13

Normozoospermia

Estop et al., 2000 [59]

53

t(5;8)

5q33;8q13

Normozoospermia

Godo et al., 2013 [7]

54

t(5;8)

5q33;8q13

Normozoospermia

Anton et al., 2008 [60]

55

t(5;8)

5q35.1;8p11.2

Astenozoospermia

Anton et al., 2008 [60]

56

t(5;8)

5q35.3;8q22.1

Recurrent fetal wastage

Fryns et al., 1998 [34]

57

t(5;9)

5p15.1;9q22.1

Normospermic, Primary infertility

Vozdova et al., 2013 [11]

58

t(5;9)

5p13;9q22

PGD

Zhang et al., 2014 [61]

59

t(5;9)

5q10;9q10

Recurrent spontaneous abortions

Rouen et al., 2017 [62]

60

t(5;9)

5q21;9q34

2 fetal losses

Adamoli et al., 1986 [37]

61

t(5;9)

5q23.2;9q22.3

Spontaneous abortion

Stephenson et al., 2006 [53]

65

t(5;9)

5q23.3;9p24

Recurrent miscarriage

Iyer et al., 2007 [63]

63

t(5;10)

5p13.3;10p12.2

PGD

Ko et al., 2010 [52]

64

t(5;10)

5q22;10q11.2

PGD

Ko et al., 2010 [52]

65

t(5;10)

5q22;10q22

Miscarriage

Sugiura-Ogasawara et al., 2008 [38]

66

t(5;10)

5q34;10p12.1

Recurrent spontaneous abortions

Rouen et al., 2017 [62]

67

t(5;10)

5q35;10q22

Spontaneous abortions

Bourrouillou et al., 1986 [64]

68

t(5;10)

5q35;10q24

Recurrent miscarriage

Goud et al., 2009 [31]

69

t(5;11)

5p14;11p15

Normozoospermia

Zhang HG et al., 2015 [5]

70

t(5;12)

5p15.1;12p12.2

Spontaneous abortion

Stephenson et al., 2006 [53]

71

t(5;12)

5p15.1;12q21

Infertility

Ravel et al., 2006 [65]

72

t(5;12)

5p14;12q15

Recurrent spontaneous abortion

Gada Saxena et al., 2012 [33]

73

t(5;12)

5q11;12p13

10 abortions

Al-Hussain et al., 2000 [54]

74

t(5;12)

5q13;12q13

Recurrent spontaneous abortions

Rouen et al., 2017 [62]

75

t(5;12)

5q35.1;12q24.1

Repeated miscarriage

Goddijn et al., 2004 [66]

76

t(5;13)

5p13;13q34

Neonatal death

Zhang et al., 2006 [67]

77

t(5;13)

5q11;13q33

3 spontaneous abortions

Pellestor et al., 1989 [68]

78

t(5;13)

5q13;13q12

Normozoospermia

Zhang HG et al., 2015 [5]

79

t(5;13)

5q15;13p12

Oligozoospermia

Matsuda et al., 1992 [69]

80

t(5;13)

5q21;13q12.1

2 miscarriage, no conception

Ikuma et al., 2015 [4]

81

t(5;13)

5q33;13q12

Infertility

Mikelsaar et al., 2012 [20]

82

t(5;13)

5q34;13q33

Recurrent miscarriage

Iyer et al., 2007 [63]

83

t(5;14)

5p13;14q11.2

PGD

Zhang et al., 2014 [61]

84

t(5;14)

5p13;14q23

Spontaneous abortions

Bourrouillou et al., 1986 [64]

85

t(5;14)

5q11.2;14q32.1

Spontaneous abortion

Stephenson et al., 2006 [53]

86

t(5;15)

5p15.2;15q21.1

PGD

Ko et al., 2010 [52]

87

t(5;15)

5p13.3;15q15.3

PGD

Ko et al., 2010 [52]

88

t(5;15)

5q35;15q22

Pregnancy of PGD

Escudero et al., 2003 [70]

89

t(5;15)

5q35;15q26.2

Abnormal semen, 2 IVF-ET

Vozdova et al., 2013 [11]

90

t(5;16)

5q13; 16p13.1

Normozoospermia

Haapaniemi Kouru et al., 2017 [71]

91

t(5;16)

5q33;16p13

Recurrent pregnancy loss

Kochhar et al., 2013 [22]

92

t(5;16)

5q33.3;16p13.3

Recurrent miscarriages

Dutta et al., 2011 [50]

93

t(5;17)

5q13.2;17q21.2

infertility

Mau et al., 1997 [72]

94

t(5;17)

5q31;17p13

Normozoospermia

Anton et al., 2008 [60]

95

t(5;17)

5q33.1;17q25.3

Repeated miscarriage

Goddijn et al., 2004 [66]

96

t(5;18)

5p15;18q11.2

Spontaneous abortion

Zhang HG et al., 2015 [5]

97

t(5;18)

5p15;18q21

Malformed children

Balkan et al., 1983 [73]

98

t(5;18)

5q15;18q22

Spontaneous abortions

Soh et al., 1984 [74]

99

t(5;18)

5q15;18q23

2 fetal loss

Smith et al., 1990 [75]

100

t(5;18)

5q31.1;18q21.1

PGD

Ko et al., 2010 [52]

101

t(5;19)

5q15;19p12

Normospermic, A boy 46,XY,t(5;19)pat

Vozdova et al., 2013 [11]

102

t(5;20)

5q22;20p13

Asthenozoospermia, Habitual abortions

Vegetti et al., 2000 [32]

103

t(5;20)

5q13;20q12

Normozoospermia

Zhang HG et al., 2015 [5]

104

t(5;20)

5q22;20p12

Recurrent fetal wastage

Fryns et al., 1998 [34]

105

t(5;20)

5q31;20p13

Azoospermia

Poli et al., 2016 [18]

106

t(X;5)

Xp22.1;5p11

Azoospermia

Peschka et al., 1999 [27]

The most common breakpoint, at 5p15, was observed in 11 patients, followed by 5q13 (N = 10). Breakpoints at 5p14, 5p11, 5q13, 5q14, 5q15, 5q22, 5q31, 5q35 and 5q35.1 were found with cases of both pregestational and gestational infertility. All breakpoints were associated with gestational infertility (Table 3).
Table 3

Incidence of breakpoints on chromosome 5

Breakpoints

Number of patients with pregestational infertility

Number of patients with gestational infertility

p15.3

 

1

p15.2

 

3

p15.1

 

4

p15

 

11

p14

1

5

p13.3

 

3

p13

 

9

p12

 

2

p11

1

2

q10

 

1

q11

 

3

q11.2

 

2

q12

 

1

q13

1

9

q13.1

 

1

q13.2

 

1

q14

1

1

q15

1

4

q21

 

4

q22

2

3

q22.1

 

1

q23.1

 

1

q23.2

 

1

q23.3

 

1

q31

2

3

q31.1

 

1

q33

 

8

q33.1

 

2

q33.2

 

1

q33.3

 

3

q34

 

2

q35

1

6

q35.1

1

2

q35.3

 

2

Discussion

In clinical practice, male infertility can be broadly divided into two types of reproductive failure: pregestational and gestational infertility [16]. In the present study, nine of our cases were identified as carriers of chromosome 5 translocations, and we also reviewed 106 cases of chromosome 5 translocation reported in the literature. The breakpoints that we identified on chromosome 5 were found to be associated with pregestational or gestational infertility. One case was associated with pregestational infertility and eight cases were related to gestational infertility. Mikelsaar et al. [17] and Venkateshwari et al. [18] reported that the breakpoints at 5q33 and 5q35 in male carriers were associated with infertility. Kim et al. [19] reported that the breakpoint at 5p13 could interfere with spermatogenesis, and that breakpoints at 5q15, 5q21.2, 5q22 and 5q32 were related to recurrent abortion. To study the relationship of these breakpoints on chromosome 5 with male infertility, we analyzed recent published literature and revealed clinical features in carriers of chromosome 5 translocations. The karyotype results and clinical findings at chromosome 5 are summarized in Table 2. A common clinical feature associated with the breakpoints at 5p13, 5q33 and 5q35 was recurrent miscarriage, which was not consistent with the above reports.

Male infertility affects about 50% of couples unable to achieve pregnancy [20]. Chromosomal abnormalities are closely related to male infertility [21], and cytogenetic detection can provide valuable information for genetic counseling of infertile males [22]. Previous reports have shown that infertile men have an 8–10-fold higher prevalence of chromosomal abnormalities than fertile men [19]. Chromosomal translocation alters the complex and vital process of spermatogenesis, and leads to male infertility [20]. Chromosome 5 translocation has often been associated with male infertility or recurrent pregnancy loss [17, 18, 23].

Table 3 shows that all breakpoints were associated with gestational infertility. These cases indicated that such breakpoints were not responsible for pregestational infertility, so another breakpoint of translocation must be responsible in these individuals. For instance, two individuals with the breakpoint 5q22 were associated with pregestational infertility, and exhibited clinical features of oligoasthenoteratozoospermia and asthenozoospermia (case 47 and 102, respectively, Table 2). The corresponding breakpoints of translocation in case 47 and 102 were 8q24.1 and 20p13, respectively. Kott et al. [24] reported that the primary ciliary dyskinesia-19 (CILD19) gene (OMIM: 614,935), mapped to chromosome 8q24, was associated with asthenospermia in infertile males. Previous studies have shown that the sperm flagellar protein 1 (SPEF1) gene (OMIM: 610,674) located on chromosome 20p13 was be associated with curvature of microtubule bundles and the axoneme of sperm flagella [25]. Previous studies suggested that disruptions of CAMK4 located on chromosome 5q22.1, SPINK13 located on chromosome5q32 and the testis-specific serine/threonine kinase ( TSSK1B ) gene mapped to chromosome 5q22.2 were associated with loss of sperm function and human male infertility [8, 9, 26]. In addition, the most common breakpoint, mapped to 5p15, was associated with gestational infertility. Other breakpoints were also identified as being associated with gestational infertility. For those affected by these breakpoints, natural conception remained possible with the potential to have normal children. For example, Ikuma et al. [4] reported that the live birth rate with natural conception for translocation carriers was 65%–83% cumulatively. However, natural conception has a greater risk. The number of chromosomal unbalanced gametes is large, leading to repetitive pregnancy loss, and may have repercussions on the fertility of translocation carriers. For these carriers, informed choice should be provided during genetic counseling.

The major limitation of our present study was the relatively small number of carriers of chromosome 5 translocations. Furthermore, we did not investigate the specific molecular effects of the translocations by molecular-cytogenetic methods.

Conclusions

In the present study, 115 carriers of chromosome 5 translocations were reviewed. The most common translocation and breakpoint were t(4;5) and 5p15, respectively. All breakpoints at chromosome 5 were associated with gestational infertility. In genetic counseling, physicians should consider chromosome 5 and its breakpoints. Carriers of chromosome 5 translocations maybe choose to continue with natural conception or use available assisted reproductive technologies, such as preimplantation genetic diagnosis.

Abbreviations

AZF: 

Azoospermia factor

CAMK4: 

Ca2+/calmodulin-dependent protein kinase IV

CILD19: 

Ciliary dyskinesia-19

ISCN: 

International System for Human Cytogenetic Nomenclature

PGD: 

Preimplantation genetic diagnosis

SPEF1: 

Sperm flagellar protein 1

Spink13: 

Serine protease inhibitor, Kazal-type 13

TSSK1B: 

Testis-specific serine/threonine kinase

Declarations

Acknowledgments

We thank Charles Allan, PhD, from Liwen Bianji, Edanz Editing China (http://www.liwenbianji.cn), for editing the English text of a draft of this manuscript.

Funding

This work was supported by the Special Funds of Jilin Province Development and Reform Commission, China (2017C025).

Availability of data and materials

Data sharing not applicable to this article as no datasets were generated or analysed during the current study.

Authors’ contributions

HGZ, LLL and HBZ performed the literature search, analyzed the data and wrote the manuscript. RXW, YP and HZ collected the clinical cases and patients. HGZ and RZL are responsible for the content and writing of the paper. All authors read and approved the final manuscript.

Ethics approval and consent to participate

The study protocol was approved by the Ethics Committee of the First Hospital of Jilin University, and written informed consent was obtained from all participants. (No.2010–082)

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

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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.

Authors’ Affiliations

(1)
Center for Reproductive Medicine and Center for Prenatal Diagnosis, First Hospital, Jilin University, 71 Xinmin Street, Chaoyang District, Changchun, Jilin Province, 130021, China

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