Printer Friendly

Focal orchitis in undescended testes: discussion of pathogenetic mechanisms of tubular atrophy.

Lymphoid tissue is rare in the testis. Nevertheless, the fetal testis contains many hematopoietic foci, which are usually located in the rete testis, interlobular septa, and tunica vasculosa. (1) The number of hematopoietic cells decreases progressively during the last months of fetal life, and the cells disappear shortly after birth (except in cases of fetal chronic anoxia). In the adult testis, in addition to a few T lymphocytes present in the rete testis, interstitial macrophages are the most common cells of the immune system. (2) The number of these cells has been estimated to be as high as 25% of the number of Leydig cells. (3) Testicular macrophages are involved in immune processes, including phagocytosis and the synthesis of prostaglandins, growth factors, and cytokines. (4) In addition, a paracrine regulation of Leydig cells by macrophages has been reported. (5)

Most series of testicular biopsies from infertile men who present with oligozoospermia or who undergo vasectomy showed no inflammatory infiltrates, no plasma cells, and no increase in the number bf macrophages. (6) Focal inflammatory infiltrates consisting of mononuclear cells have been reported only in isolated series of patients with azoospermias or oligozoospermias of various etiologies. However, the incidence of these cases in such series has never been higher than 4.8%. (7)

Cryptorchid testes diagnosed in adulthood frequently contain lesions that involve all testicular structures, although the severity of lesions varies widely. (8) Some authors assume that these lesions are primary (dysgenetic), whereas other authors maintain that the lesions are secondary to increased temperature. (9) Among these lesions, no reference to inflammatory infiltrates has been reported. The aim of the present report was to describe the presence of lymphoid infiltrates in seminiferous tubules and interstitium (a lesion described by the term focal orchitis) of adult cryptorchid testes and to evaluate the role of this lesion in the mechanism that leads to tubular atrophy.

MATERIALS AND METHODS

We obtained clinical personal histories of 50 men with cryptorchidism who underwent orchidectomy of their cryptorchid testes in La Paz Hospital, and we reviewed the histologic sections of these removed testes. Twenty-two (44%) of these patients had lymphoid infiltrates in the seminiferous tubules and interstitium of their removed testes and were selected for the study. All of these patients presented with unilateral cryptorchidism. After orchidectomy, the testes had been cross sectioned into 2-mm-wide slides (blocks) fixed in Bouin fixative and embedded in paraffin. Cross sections (6 [micro]m thick) of each slide had been performed and stained with hematoxylin-eosin. For this study, 3 new histologic sections (6 [micro]m thick) were obtained from each slide and stained with hematoxylin-eosin, Masson trichrome, or orcein (for demonstration of elastic fibers).

The histologic study of the removed testes and epididymides included the following evaluations: (1) seminiferous tubule pathology: hypospermatogenesis (complete spermatogenesis although the numbers of all cell types are very low), maturation arrest of spermatogenesis (at the level of spermatogonia, spermatocytes, or spermatids), intratubular germ cell neoplasia, Sertoli cell-only tubules, hyalinized tubules, or mixed atrophy of the testis (coexistence of Sertoli cell-only tubules and tubules with complete or incomplete spermatogenesis) (9,10) ; (2) Sertoli cell pattern, evaluated according to Nistal et al (11,12) as normal adult (triangle-shaped, irregularly outlined nucleus with a prominent centrally located nucleolus), dysgenetic (anomalous maturation, displaying an ovoid, regularly outlined nucleus with small, dense chromatin granules and a normal nucleolus), or granular (numerous eosinophil granules--which are lysosomes--in the apical cytoplasm); (3) tubular lumen (normal or ectatic tubules); (4) type and characteristics of inflammatory infiltrates: lymphocytes, neutrophils, or macrophages; (5) rete testis pattern: normal or cystic hypoplasia; and (6) epididymal pattern: normal or epididymal duct hypoplasia (low epithelium, thin muscular wall, and dilated lumen).

An immunohistochemical study with antibodies against immune system cell markers (CDs) was carried out according to the avidin-biotin-peroxidase method in histologic sections of each testis. The antibodies used and their respective antigens were CD3 (T lymphocytes) (Novocastra, Barcelona, Spain); CD15 (neutrophils) (Concepta, Barcelona, Spain); CD20 (B lymphocytes) (Dako, Glostrup, Denmark); and CD68 (macrophages) (Dako).

RESULTS

The results are summarized in Tables 1 and 2. Cryptorchidism was unilateral in the 22 patients. The undescended testes were located in the right side in 12 patients (55%) and in the left side in 10 patients (45%). Cryptorchidism was inguinal in 18 patients (82%) and abdominal in 4 patients (18%). The patients had a mean [+ or -] SD age of 32.7 [+ or -] 18.5 years (range, 14-88 years).

The results of the routine preoperative laboratory analysis (including hematologic and biochemical assays) were normal. The radiologic findings and the findings of other imaging studies of the subsequently removed cryptorchid testes were unremarkable. No antecedents of orchitis, infectious disease, or orchidectomy had been recorded in the patients' histories.

In all of the cases, inflammatory infiltrates were focal and multiple. The infiltrates were present in both the testicular interstitium (Figure 1) and the seminiferous tubules in about half of the slices (blocks), usually in all sections from these slices, and they occupied from 10% to 30% of the surface area of the section. In general, the inflammatory infiltrates consisted of lymphocytes, macrophages, plasma cells, eosinophils, and mast cells. The predominant cell types in the inflammatory infiltrates were lymphocytes in 20 testes (90%) and neutrophils in 2 testes (Figure 2). The immunohistochemical study revealed that in 18 of the 20 cases showing a predominance of lymphocytes, these lymphocytes were mainly T lymphocytes (CD3-positive cells) (Figure 3), whereas in the other 2 cases, the infiltrate was granulomatous and consisted of T lymphocytes (CD3-positive cells), B lymphocytes (CD20-positive cells), plasma cells, and macrophages (Table 2).

[FIGURES 1-3 OMITTED]

The histopathologic diagnoses of the testes according to the seminiferous tubule pathology were mixed atrophy (11 testes, 50%, 4 of which also showed hyalinized tubules); Sertoli cell-only tubules plus hyalinized tubules (4 testes, 18.2%); Sertoli cell-only tubules (3 testes, 13.6%); intratubular germ cell neoplasia (2 testes, 9%, 1 of which also showed intermingled hyalinized tubules); complete tubular hyalinization (1 testis, 4.5%); and tubular hyalinization plus some groups of tubules with hypospermatogenesis (1 testis, 4.5%) (Table 1).

Multiple histologic patterns were noted in the seminiferous tubules that contained inflammatory infiltrates or in the tubules adjacent to the interstitial inflammatory infiltrates: hypospermatogenesis (1 testis) (Figure 4); spermatogonial maturation arrest (2 testes) (Figure 1); tubules with intratubular germ cell neoplasia (1 testis) (Figure 5); Sertoli cell-only tubules (16 testes) (Figures 2 and 6); hyalinized tubules (10 testes, 9 of which also showed inflammatory infiltrates in other tubule types [Sertoli cell-only tubules in 7 testes, tubules with intratubular germ cell neoplasia in 1 testis, and tubules with hypospermatogenesis in 1 testis]) (Table 2).

[FIGURES 4-6 OMITTED]

In the 11 testes with mixed atrophy, Sertoli cell-only tubules were intermingled with tubules showing maturation arrest of spermatogonia (Table 1). In addition, 4 of these testes also had hyalinized tubules. In the other 7 testes, the Sertoli cell-only tubules occupied from 40% to 99% of the testicular parenchyma. All testes with mixed atrophy had dysgenetic Sertoli cells (Figures 2 and 6), although normal mature Sertoli cells were also found in 3 of these testes. Granular Sertoli cells were observed in 7 testes with mixed atrophy, although in 2 of these testes, the granular changes appeared in tubules with inflammatory infiltrates.

In 6 of the 11 testes showing hyalinized tubules (27% of all testes studied), these tubules occupied from 20% to 100% of testicular parenchyma. In 10 testes (45%), the focal orchitis was present in the hyalinized tubules.

Tubular ectasia was observed in 13 testes (59%). The percentage of testicular parenchyma occupied by the ectatic tubules varied from 2% to 80%. The 8 testes (36%) showing tubular ectasia in more than 20% of testicular parenchyma had mixed atrophy. In 9 testes (40.9%), the ectatic tubules showed inflammatory infiltrates in the tubular wall and/or in the adjacent interstitial tissue.

In 6 testes (27%), the Leydig cells formed large clusters resulting in apparent hyperplasia. In 3 testes (13.6%), lymphocytes were found among the Leydig cells.

The rete testis was hypoplastic and showed cystic transformation in 18 testes (81%). In 11 of these testes (50% of all testes studied), ectasia of the rete testis was also observed. The epididymis was hypoplastic in 15 testes (68%).

COMMENT

The adult undescended testes included in this study had multiple interstitial and tubular inflammatory infiltrates with destruction of some seminiferous tubules. These histopathologic findings are collectively called focal orchitis. Although no clinical evidence of inflammation was present, the term focal orchitis has been used in the literature to describe this pathologic entity. (13-16) The occurrence of lymphoid cell infiltrates in the testis has been reported in experimental studies in laboratory animals. (13,14) In the human testis, inflammatory cells have been found in association with degenerating tubules in elderly men (15-17) and also in a small number of biopsies performed in infertile patients. (6,7) This lesion, named focal orchitis by Honore, (16) has been explained as an autoimmune process produced by an alteration of the blood-testis barrier that permits the passage of antigens from the adluminal tubular compartment to the testicular interstitium. (18) The cause of this alteration in elderly men might be 2 disorders that are frequent in these men: Sertoli cell loss (19) and seminiferous tubule degeneration. (20) Rupture of the blood-testis barrier would be responsible for the high percentage of adult men with serum antibodies that react against spermatozoa and cause autoimmune lesions (21) that, in infertile patients, give rise to immune deposits in the tubular wall or in the basement membrane of seminiferous tubules. (22)

The development of focal orchitis in cryptorchid testes has been reported in experimental cryptorchidism in laboratory animals. The inflammatory infiltrates observed in these laboratory animals consisted of mononuclear leukocytes with a few eosinophils, and these infiltrates appeared around the seminiferous tubules. (13) It has been assumed that these lesions are very similar to those observed in experimental autoimmune orchitis and that eventually, the lesions can cause complete tubular hyalinization. (23)

The incidence of focal orchitis in human cryptorchid testes and its possible involvement in seminiferous tubule atrophy are unknown. It is more difficult to determine the etiology of testicular atrophy in undescended testes in men than in laboratory animals subjected to experimental cryptorchidism because laboratory animals have normal testes before the experiment, whereas in humans with congenital cryptorchidism, it is possible that the testes had lesions other than cryptorchidism itself, possibly congenital lesions, and that the severity of these lesions varies widely.

The presence of congenital lesions in cryptorchidism is supported by the following findings: (1) patients with the same type of cryptorchidism (inguinal, abdominal, or high scrotal) and the same age can show very different germ cell numbers; (2) postpubertal biopsies of testes that were surgically descended in infancy have revealed a great variability of seminiferous epithelium lesions including spermatogonial maturation arrest, Sertoli cell-only tubules with dysgenetic Sertoli cells, tubular hyalinization, and mixed atrophy (8); and (3) the study of removed testes has shown a deficient maturation of both the rete testis and the epididymis, an alteration that might cause anatomical or functional obstruction of the sperm excretory ducts. (24) If prolonged exposure to high temperature were the only cause of spermatogenetic lesion in human cryptorchidism, as occurs in experimental cryptorchidism, the lesions should be diffuse and should be equally severe in all of the seminiferous tubules. The diffuse lesions of the germinal epithelium observed here were those to be expected in adult undescended testes: a high incidence of mixed atrophy, followed by Sertoli cell-only tubules combined with tubular hyalinization, Sertoli cell-only tubules, intratubular germ cell neoplasia, complete hyalinization, and focal spermatogenesis.

There were several interesting findings in the present study, including a high incidence of focal orchitis in adult cryptorchidism (44%), the apparent absence of symptoms during the development of focal orchitis, and the normality of laboratory data. The elevated frequency of focal orchitis can be explained in 2 different ways: (1) the exhaustive study performed in entire testes has rendered a high number of cases, whereas testicular biopsies may not be representative; and (2) the altered Sertoli cells in cryptorchid testes may have deficient synthesis of factors involved in the regulation of immune processes. (25)

In the 2 patients with intratubular germ cell neoplasia, the orchitis was possibly related to these tumor cells. (26) In the remaining 20 patients, the causes seem to be more complex, and other alterations in the seminiferous tubules should be taken into account. These alterations include tubular ectasia, dysgenetic Sertoli cells, and Sertoli cells with granular changes.

Tubular ectasia is secondary to rete testis dysgenesis (a frequent finding in cryptorchid testes), hypoplasia of the epididymis, (27) or other epididymal malformations. In the present study, an increased incidence of both cystic hypoplasia of the rete testis and epididymal hypoplasia were observed (81% and 68%, respectively). The increased intratubular pressure in tubular ectasia probably caused the atrophy of the seminiferous epithelium with subsequent injury of the Sertoli cells, which were often dysgenetic. It is possible that these Sertoli cell lesions lead to a disruption of the blood-testis barrier, allowing the subsequent passage of antigens from the tubular lumen to the testicular interstitium. The antigens that would provoke this immune response in the testis could be released by germ cells of the adluminal compartment (in testes with complete spermatogenesis), (28) tumor cells (in testes with intratubular germ cell neoplasia), or anomalous dysgenetic Sertoli cells.

However, tubular ectasia itself was not the sole cause of orchitis in all of the cases, inasmuch as it was remarkable in only 36% of the cryptorchid testes with focal orchitis. Dysgenetic Sertoli cells (Sertoli cells that have undergone anomalous, incomplete maturation (29)) were observed in all nonhyalinized seminiferous tubules with inflammatory infiltrates. Since normal Sertoli cell maturation is required for the development and maintenance of the blood-testis barrier (30) and these cells seem to play an important role in immunosuppression, (31) the Sertoli cell dysgenesis might be an important cause of the focal orchitis observed in this study.

In the present study, Sertoli cells with granular cytoplasm were occasionally observed in tubules with inflammatory infiltrates (9% of testes studied), and thus, their association with the orchitis process is not consistent. In addition, no reference to inflammatory infiltrates was found in a previous study of these anomalous Sertoli cells. (12)

In summary, focal orchitis is a common finding in undescended testes. Focal orchitis, together with other factors such as ischemia and hormonal deprivation, may be one of the factors leading to tubular hyalinization. The causes of this orchitis are unknown, but the process may result from multiple single factors. Among these factors, tubular ectasia and Sertoli cell dysgenesis might play a role by disrupting the blood-testis barrier, allowing antigens to enter the testicular interstitium and giving rise to an autoimmune process.
Table 1. Histologic Findings in 22 Adult Cryptorchid Testes With
Focal Orchitis

 Loca- Tubules Without Inflammatory Infiltrates
 tion
 Age, and Histopathologic Sertoli Cell
Case y Side * Diagnosis Pattern

 1 22 I, R Mixed atrophy (50% Dysgenetic
 spermatogonial arrest + + mature
 50% Sertoli cell only) + granular
 2 14 I, R Mixed atrophy (50% Dysgenetic
 spermatogonial arrest + + mature
 50% Sertoli cell only)
 3 20 I, L Mixed atrophy (60% Dysgenetic
 spermatogonial arrest +
 40% Sertoli cell only)
 4 36 I, L Mixed atrophy (20% Dysgenetic
 spermatogonial arrest +
 80% Sertoli cell only)
 5 20 I, R Mixed atrophy (20% Dysgenetic
 spermatogonial arrest + + granular
 80% Sertoli cell only)
 6 16 I, R Mixed atrophy (1% Dysgenetic
 spermatogonial arrest + + granular
 99% Sertoli cell only)
 7 21 I, L Mixed atrophy (1% Dysgenetic
 spermatogonial arrest + + granular
 99% Sertoli cell only)
 8 36 I, R Mixed atrophy (5% sper- Dysgenetic
 matogonial arrest + 5% + granular
 Sertoli cell only +
 90% hyalinized)
 9 48 I, R Mixed atrophy (5% sper- Dysgenetic
 matogonial arrest + 15% + granular
 Sertoli cell only +
 80% hyalinized)
 10 32 I, R Mixed atrophy (80% Dysgenetic
 spermatogonial arrest + + mature
 18% Sertoli cell only + + granular
 2% hyalinized
 11 34 I, L Mixed atrophy (98% Dysgenetic
 spermatogonial arrest +
 1% Sertoli cell only +
 1% hyalinized)
 12 75 I, R 90% Sertoli cell only + Dysgenetic
 10% hyalinized
 13 20 I, L 90% Sertoli cell only + Dysgenetic
 10% hyalinized
 14 47 A, L 40% Sertoli cell only + Dysgenetic
 60% hyalinized
 15 39 I, L 50% Sertoli cell only + Dysgenetic
 50% hyalinized
 16 20 I, L 100% Sertoli cell only Dysgenetic
 17 20 I, L 100% Sertoli cell only Dysgenetic
 18 34 A, L 100% Sertoli cell only Dysgenetic
 19 29 A, R 100% Intratubular germ Dysgenetic
 cell neoplasia + mature
 20 27 I, R 50% Intratubular germ Dysgenetic
 cell neoplasia + 50%
 hyalinized
 21 88 A, R 100% hyalinized ...
 22 23 I, R 80% Hyalinized with Dysgenetic
 spermatocele + 20% + mature
 hypospermatogenesis

 Tubular
 Ectasia, %
Case ([dagger]) Rete Testis Epididymis

 1 60 Cystic hypoplasia Hypoplastic
 2 30 Cystic hypoplasia Hypoplastic
 3 22 Normal Dilated
 4 80 Cystic hypoplasia Hypoplastic
 5 50 Cystic hypoplasia Hypoplastic
 6 50 Cystic hypoplasia Hypoplastic
 7 ... Cystic hypoplasia Normal
 8 2 Normal Hypoplastic
 9 5 Cystic hypoplasia Hypoplastic
 10 30 Cystic hypoplasia Hypoplastic
 11 60 Cystic hypoplasia Hypoplastic
 12 ... Cystic hypoplasia Normal
 13 ... Normal Normal
 14 ... Cystic hypoplasia Hypoplastic
 15 5 Cystic hypoplasia Normal
 16 ... Cystic hypoplasia Hypoplastic
 17 5 Cystic hypoplasia Hypoplastic

 18 ... Cystic hypoplasia Hypoplastic
 19 ... Cystic hypoplasia Hypoplastic
 20 ... Normal Normal
 21 ... Cystic hypoplasia Hypoplastic
 22 18 Cystic hypoplasia Normal

* I indicates inguinal; A, abdominal; R, right; and L, left.

([dagger]) Percentage of testicular parenchyma surface area
showing tubular ectasia.
Table 2. Histologic Findings in Tubules With Inflammatory
Infiltrates in 22 Adult Cryptorchid Testes With Focal Orchitis

 Tubules With Inflammatory
 Infiltrates

 Histopathologic Sertoli Cell Inflammatory
Case Diagnosis Pattern Infiltrate

 1 Spermatogonial Dysgenetic + T lymphocytes
 arrest mature +
 granular
 2 Spermatogonial Dysgenetic T lymphocytes
 arrest
 3 Sertoli cell only Dysgenetic Neutrophils
 4 Sertoli cell only Dysgenetic T lymphocytes
 5 Sertoli cell only Dysgenetic + Neutrophils
 granular
 6 Sertoli cell only Dysgenetic T lymphocytes
 7 Sertoli cell only Dysgenetic T lymphocytes
 8 Sertoli cell only + Dysgenetic T lymphocytes
 hyalinized
 9 Sertoli cell only + Dysgenetic T lymphocytes
 hyalinized
 10 Sertoli cell only + Dysgenetic + T lymphocytes
 hyalinized mature
 11 Sertoli cell only + Dysgenetic T lymphocytes
 hyalinized
 12 Sertoli cell only + Dysgenetlc T lymphocytes
 hyalinized
 13 Sertoli cell only Dysgenetic T lymphocytes
 14 Sertoli cell only + Dysgenetic T lymphocytes
 hyalinized
 15 Sertoli cell only + Dysgenetic T lymphocytes
 hyalinized
 16 Sertoli cell only Dysgenetic T lymphocytes
 17 Sertoli cell only Dysgenetic T lymphocytes
 18 Sertoli cell only Dysgenetic T lymphocytes
 19 Intratubular germ Dysgenetic T and B lymphocytes +
 cell neoplasia macrophages + plasma
 cells
 20 Intratubular germ Dysgenetic T and B lymphocytes +
 cell neoplasia + macrophages
 hyalinized + plasma cells
 21 Hyalinized ... T lymphocytes
 22 Hypospermatogenesis Dysgenetic + T lymphocytes
 + hyalinized mature
 with spermatocele


This work was supported by grants from the Fondo de Investigaciones Sanitarias de la Seguridad Social.

Accepted for publication August 28, 2001.

From the Department of Morphology, School of Medicine, Autonomous University, Madrid, Spain (Drs Nistal and Riestra); the Department of Pathology, La Paz Hospital, Madrid (Dr Nistal); and the Department of Cell Biology and Genetics, University of Alcala, Madrid (Dr Paniagua).

Reprints: Manuel Nistal, MD, Department of Morphology, School of Medicine, Autonomous University, Calle Arzobispo Morcillo 2, E-28029 Madrid, Spain.

References

(1.) Nistal M, Paniagua R. Development of the testis from birth to puberty. In: Nistal M, Paniagua R, eds. Testicular and Epididymal Pathology. New York: Thieme-Stratton Inc; 1984:14-25.

(2.) El-Demiry MI, Hargreave TB, Busuttil A, Elton R, James K, Chisholm GD. Immunocompetent cells in human testis in health and disease. Fertil Steril. 1987; 48:470-479.

(3.) Hutson JC. Testicular macrophages. Int Rev Cytol. 1994;149:99-143.

(4.) Yee JB, Hutson JC. Testicular macrophages: isolation, characterization and hormonal responsiveness. Biol Reprod. 1983;29:1319-1326.

(5.) Afane M, Dubost JJ, Sauvezie B, et al. Modulation of Leydig cell testosterone production by secretory products of macrophages. Andrologia. 1998;130:71-78.

(6.) Hendry WF, Levison DA, Parkinson MC. Testicular obstruction: clinicopathological studies. Ann R Coll Surg Engl. 1990;72:396-407.

(7.) Suominen J, Soderstrom KO. Lymphocyte infiltration in human testicular biopsies. Int J Androl. 1982;5:461-466.

(8.) Nistal M, Paniagua R. Non-neoplastic diseases of the testis. In: Bostwick DG, Eble JN, eds. Urologic Surgical Pathology. St Louis, Mo: Mosby; 1977:481-485.

(9.) Nistal M, Paniagua R, Diez-Pardo JA. Histological classification of undescended testes. Hum Pathol. 1980;11:666-674.

(10.) Nistal M, Paniagua R. Testicular biopsy. Contemporary interpretation. Urol Clin North Am. 1999;26:555-593.

(11.) Nistal M, Jimenez F, Paniagua R. Sertoli cell types in Sertoli-cell-only syndrome: relationship between Sertoli cell morphology and aetiology. Histopathology. 1990;15:173-180.

(12.) Nistal M, Garcia-Rodeja E, Paniagua R. Granular transformation of Sertoli cells in testicular disorders. Hum Pathol. 1991;22:131-137.

(13.) Scott JN, Fritz HI, Nagy F. Response to cryptorchidism of the testis and epididymis of the opossum (Didelphis virginiana). J Reprod Fertil. 1979;57:175-178.

(14.) Tung KS, Ellis L, Teuscher C, et al. The lack mink (Mustela vison). A natural model of immunologic male infertility. J Exp Med. 1981;154:1016-1032.

(15.) Frick J. Darstellung einer Methode zur Bestimmung des Testosteronspiegels im Plasma und Studie uber den Testosteronmetabolismus beim Mann uber 60 Jahre. Urol Int. 1969;24:481-501.

(16.) Honore LH. Aging changes in the human testis: a light-microscopic study. Gerontology. 1978;24:58-65.

(17.) Suoranta H. Changes in the small blood vessels of the adult human testis in relation to age and some pathological conditions. Virchows Arch. 1971;352: 165-181.

(18.) Johnson L. Evaluation of the human testis and its age-related dysfunction. Prog Clin Biol Res. 1989;302:35-60.

(19.) Johnson L, Zane RS, Petty CS, Neaves WB. Quantification of the human Sertoli cell population: its distribution, relation to germ cell numbers, and age-related decline. Biol Reprod. 1984;31:785-795.

(20.) Harman SM. Clinical aspects of aging of the male reproductive system. In: Schneider El, ed. The Aging Reproductive System. Vol 4. New York, NY: Raven Press; 1978:29-58.

(21.) Fjallbrant B. Autoimmune human sperm antibodies and age in males. J Reprod Fertil. 1975;43:145-148.

(22.) Salomon F, Saremaslani P, Jakob M, Hedinger CE. Immune complex orchitis in infertile men. Immunoelectron microscopy of abnormal basement membrane structures. Lab Invest. 1982;47:555-567.

(23.) Padmanabhan R, Singh S. Effect of experimental cryptorchidism on the testis in the rat--a histological study. Z Mikrosk Anat Forsch. 1981;95:1057-1064.

(24.) Nistal M, Jimenez-Heffernan JA. Rete testis dysgenesis. A characteristic lesion of undescended testes. Arch Pathol Lab Med. 1997;121:259-264.

(25.) Turek PJ, Malkowicz SB, Tomaszewski JE, Wein AJ, Peehl D. The role of the Sertoli cell in active immunosuppression in the human testis. Br J Urol. 1996; 77:891-895.

(26.) Schutte B, Holstein AF, Schirren C. Macrophages lysing seminoma cells in patients with carcinoma-in-situ (CIS) of the testis. Andrologia. 1988;20:295-303.

(27.) Mollaeian M, Mehrabi V, Elahi B. Significance of epididymal and ductal anomalies associated with undescended testis: study in 852 cases. Urology. 1994; 43:857-860.

(28.) Soderstrom KO, Anderson LC. Identification of the auto-antigen-expressing cells in the rat testis. Exp Mol Pathol. 1981;35:332-337.

(29.) Nistal M, Paniagua R, Abaurrea MA, Santamaria L. Hyperplasia and the immature appearance of Sertoli cells in primary testicular disorders. Hum Pathol. 1982;13:3-12.

(30.) Cavicchia JC, Sacerdote FL, Ortiz L. The human blood-testis barrier in impaired spermatogenesis. Ultrastruct Pathol. 1996;20:211-218.

(31.) Willing AE, Cameron DF, Sanberg PR. Sertoli cell transplants: their use in the treatment of neurodegenerative disease. Mol Med Today. 1998;4:471-477.
COPYRIGHT 2002 College of American Pathologists
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2002 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Nistal, Manuel; Riestra, Maria Luisa; Paniagua, Ricardo
Publication:Archives of Pathology & Laboratory Medicine
Geographic Code:4EUSP
Date:Jan 1, 2002
Words:3886
Previous Article:Use of FTA Gene Guard filter paper for the storage and transportation of tumor cells for molecular testing.
Next Article:Coincident choroid plexus carcinoma and adrenocortical carcinoma with elevated p53 expression: a case report of an 18-month-old boy with no family...
Topics:


Related Articles
Health Zone: Have I got ORCHITIS.. HYPOCHONDRIAC CORNER ..or TESTICULAR CANCER?
Miriam Stoppard advice column: Girls leave me speechless..
Living: Health: Doctor David.
family health.
Abnormalities of Sexual Development in Male Rats with in Utero and Lactational Exposure to the Antiandrogenic Plasticizer Di(2-ethylhexyl) Phthalate.
Pet problems.
Duplication of the testis with contralateral anorchism.
Ultrasound of the acute scrotum.

Terms of use | Copyright © 2017 Farlex, Inc. | Feedback | For webmasters