The human oviduct, also known as the fallopian tube, is an essential component of the normal reproductive process. The tube, which connects the peritoneal space to the endometrial cavity, captures the egg after ovulation and transports the sperm from the uterus to the fertilization site in the ampulla (the middle portion of the tube). The ampulla serves as the physiologic site for final gamete maturation, fertilization, and early embryonic development. This article reviews the morphologic, physiologic, functional, and pathologic aspects of the human oviduct.
Early in the embryologic life, 2 sets of paired genital ducts exist: the wolffian ducts (mesonephric duct) and the müllerian ducts (paramesonephric duct). At about 6 weeks’ gestation, the wolffian ducts regress in females because testosterone and müllerian inhibiting substance (MIS) are not secreted in the absence of testis. The müllerian ducts develop into the female genital tract in a cephalocaudal fashion. The more cephalad ends of the paired paramesonephric ducts are opened to the peritoneal cavity and develop into the fallopian tubes, while the more caudal portion fuses in the lower midline to form the uterovaginal primordium, which later develops into the epithelium and glands of the uterus and cervix.1
If one müllerian duct fails to develop (usually associated with lack of development of the mesonephric system on the same side), a unicornuate uterus results, which consists of one uterine horn with only one fallopian tube. Complete failure of the müllerian system results in the absence of the fallopian tubes, the uterus, the cervix, and most of the vagina (Rokitansky-Küster-Hauser syndrome). Remnants of the paramesonephric duct develop as paratubal cysts or hydatid cysts of Morgagni.
The paired fallopian tubes extend laterally from the cornua of the uterus on each side and end near the ovaries. They range in length from 10-14 cm and are about 1 cm in external diameter, connecting the peritoneal space to the endometrial cavity. The ostia or openings of the tube are about 1.5 mm in diameter at the cornual end and 3 mm in diameter at the peritoneal end. The tubes sit within the abdominal cavity and are suspended by the mesosalpinx, a free edge of the superior portion of the broad ligament that contains the blood supply and nerves.2, 3 Except for their intramural part, the tubes are covered by the peritoneum.
For descriptive purposes, each fallopian tube is divided into 4 anatomic regions.
The infundibulum, from the Latin word meaning funnel, is the funnel-shaped most distal end of the tube and is in close relation to the ovary. The peritoneal ostium lies at the base of the infundibulum and is surrounded by 20-30 irregular fingerlike projections (fimbriae), which spread over the surface of the ovary, and a single large fimbria (the fimbria ovarica), which is attached to the ovary. The fimbriae trap the ovulated ovum and sweep it through the tubal ostium into the ampulla.4 The infundibulum is surrounded by a thin longitudinal muscular layer.
The ampulla is about 4-6 cm in length and is the longest region of the tube, comprising about half its length. It is also the widest region, about 6 mm in inner diameter, and the most tortuous region. Its luminal diameter is wider at its distal end than its proximal end. It is relatively thin walled and surrounded by 2 smooth muscle layers, an inner longitudinal layer and an outer circular layer. Fertilization occurs in this region.
The isthmus is short, about 2.5-4 cm, and begins as the tube exits the uterus. Its lumen is narrow, about 1-2 mm in diameter, and the muscular wall is thick and well developed, consisting of 3 well-defined layers: an inner longitudinal layer, an outer longitudinal layer, and a middle circular layer.5, 6
The interstitial or intramural segment is 1-2 cm long and constitutes the uterine-tubal junction. This section extends through the wall of the uterus and the ostium opens within the uterine cavity.
Complex coordinated contractions of the musculature are thought to be important for movement of the ovum from the distal end to the proximal end of the tube, while at the same time aiding in the movement of sperm from the proximal end to the distal end of the oviduct.
Arterial supply to the tubes is derived from the uterine and ovarian arteries, with the uterine branches supplying the medial two thirds of the tube. The tubal branches traverse and anastomose between the layers of the mesosalpinx. The venous system follows a similar path, draining into the uterine and ovarian veins. The lymphatic system follows the lymphatic drainage of the uterine fundus and the ovary, ascending along the ovarian veins and draining into the internal iliac and the aortic lymph nodes in the lumbar region. The tubes are innervated by both sympathetic and parasympathetic nerves, derived partly from the ovarian plexus and partly from the uterine plexus, and by afferent nerves contained in T11, T12, and L1 nerves.3, 7
The lumen of the oviduct is formed by a complex interdigitating system of longitudinal mucosal folds (plicae), lined by mucosal and underlying stromal connective tissue.6 Plicae are most prominent in the ampullary region and least prominent in the isthmic region. The stroma is thin, but the lamina propria is thick, with vascular channels between the epithelial and muscular layers. The adventitia contains blood vessels and nerves between the muscular layer and the peritoneal surface.
Three different cell types are present in the mucosa of the oviduct. Columnar ciliated epithelial cells are most prominent near the ovarian end and constitute 25% of the mucosal cells. Secretory cells constitute 60% of the mucosa and are mostly in the isthmic region. Narrow peg cells are located between secretory and ciliated cells and are believed to be a variant of secretory cells.7
The morphology of the epithelium is controlled by female hormones.8, 9, 10 During the follicular phase, rising estrogen levels stimulate differentiation of the epithelium into secretory and ciliated cells. At the time of ovulation, approximately half of the epithelial cells lining the oviductal lumen are secretory cells. The apical tips of these cells contain secretory granules that release their secretory products by exocytosis.
Estrogen induces both hypertrophy as well as hyperplasia of the oviductal epithelium. It stimulates the differentiation of the secretory cells, the development of the secretory organelles, and ciliogenesis. Progesterone antagonizes these processes, resulting in atrophy, regression, and loss of cilia and secretory activity. As with other reproductive tract tissues, estrogen and progesterone regulate these processes in part by regulation of their own receptor levels. Estrogen stimulates the production of both estrogen and progesterone receptors while progesterone has an opposite, suppressive effect on both receptors in the oviduct.11, 12
The lumen of the oviduct is filled with fluid composed of a complex mixture of oviduct-specific secretory proteins, selective serum transudate, and electrolytes.13 Albumin, immunoglobulins, and transferrin are the primary serum proteins present within oviductal fluid. While a number of other proteins, such as growth factors, enzymes, protease inhibitors, and cytokines, have also been identified in oviductal fluid, only one oviduct-specific molecule has been well characterized to date. At the time of ovulation, the major oviduct-specific protein present in oviductal fluid is oviductal glycoprotein (OGP).8
OGP is an estrogen-dependent glycoprotein that is synthesized and secreted by the secretory cells of the human oviduct.14, 15 OGP is species-specific but shares a certain homology. Studies suggest that OGP is a sialomucin involved in forming a protective barrier due to its relative resistance to proteolytic degradation.16
The physiologic function of OGP is not known; however, evidence suggests that OGP is involved in fertilization and potentially in the early embryonic development processes. It has been found to be associated with the zona pellucida (ZP) and the flocculent material present within the perivitelline space of oviductal eggs and embryos but not associated with ovarian eggs.17, 18, 19, 20, 21, 22, 23 Also, inclusion of OGP in in vitro sperm binding and in vitro fertilization (IVF) assays enhances sperm binding to the ZP, increases sperm penetration through the ZP, and increases the fertilization rate.23, 24, 25, 26 Addition of antibodies directed specifically against OGP has reversed or inhibited the effects of OGP on sperm binding and fertilization.27
A limited number of reports are available on OGP effects on embryonic development. These studies suggest that OGP may enhance embryo cleavage rates and blastocyst formation. As a whole, the functional studies on OGP strongly support the contention that OGP may play a role as an enhancing factor in key reproductive events. Moreover, some hypothesize that the addition of OGP to procedures may lead to better overall outcomes.28, 29
In addition to its contribution of oviductal secretions, the oviduct serves as an important reservoir for sperm. Numerous studies have shown that sperm are retained within the isthmic portion of the oviduct. Of the millions of sperm present within a normal ejaculate, only thousands enter the isthmus and only a select few reach the site of fertilization in the ampulla. As sperm enter the isthmus, many of them adhere to the epithelium.30, 31, 32, 33 This adherence may be promoted by the extremely narrow lumen at the uterine end of the isthmus, thus providing a greater chance of contact between the sperm and the mucosa.
Studies have shown that incapacitated sperm bind with higher affinity than capacitated sperm.34, 35, 36 In both in vivo studies and in vitro studies, the interaction of sperm with oviductal epithelial cells has been shown to enhance sperm viability, stabilize the acrosomal membrane, and potentially prevent or reduce polyspermy.37, 38, 39, 40 Sperm-epithelial interaction decreases as sperm become capacitated. This may be due to changes in molecules present on the sperm plasma membrane as well as hyperactivated motility of sperm in a capacitated state, which allows them to detach more easily.37, 38 Soluble factors produced by oviductal cells may in part account for some of the positive effects of epithelial cells on sperm.41 Sperm appear to bind to species-specific carbohydrates present on the surface of oviductal cells via a lectinlike mechanism. As sperm capacitate, this lectin appears to be lost or masked.
Salpingitis is the inflammation of the fallopian tube, most commonly caused by an infection. Acute salpingitis is often used synonymously with pelvic inflammatory disease (PID) because it is the most common form of PID and because the most common and serious long-term sequelae of PID involve the tubes.
Salpingitis is the most common serious infection in women of reproductive age. An estimated 1 million new cases occur in the United States every year, most commonly in females aged 15-25 years, and about 1-2% of sexually active young women are affected annually. However, the true incidence of acute salpingitis is not known because no precise definition of the disease exists and many cases are subclinical.42, 43, 44, 45
Acute salpingitis and its sequelae cause a substantial public health burden. In 1994, the total cost of PIDs exceeded $4 billion and the projected total annual cost for the year 2000 was $10 billion. However, since that time, the hospitalization rate has declined due to changes in the criteria for hospital admissions, an increase in outpatient management, and a decrease in incidence of PID. Rein et al estimated that the direct cost of PID and its sequelae was $1.88 billion in 1998.7, 46, 47, 48 The decline in PID incidence might be attributable to an expansion of national and regional programs that screen women for asymptomatic chlamydial infections, one common cause of PID.49
Risk factors for acquiring acute salpingitis are similar to those for acquiring sexually transmitted diseases (STDs). Age is inversely related to the rate of acute salpingitis and directly related to long-term sequelae. Sexually active teenagers are 3 times more at risk for acquiring acute salpingitis than women aged 25-29 years. This is due to the biologic and behavioral characteristics of this age group, such as young age at first sexual intercourse, multiple sexual partners, high frequency of unprotected sexual intercourse, and increased rate of acquiring new partners within 30 days.50, 43, 51, 52, 53
Other risk factors that have been associated with acute salpingitis include never being married, divorced or separated, and low socioeconomic status as measured by lower level of education, lower income, or unemployment.54
Neisseria gonorrhoeae and Chlamydia trachomatis were originally thought to be the only pathogens that caused acute salpingitis until investigators used laparoscopy to collect specimen from patients with PID. Culture results revealed that N gonorrhoeae and C trachomatis were inconsistently recovered: C trachomatis was recovered from the cervix in 5-39% of patients with PID and from the fallopian tubes in only 0-10%; similarly, N gonorrhoeae was isolated from the cervix in 27-80% of cases and from the fallopian tubes in only 13-18% of cases. This is probably because of variations among the populations studied and the severity of infection, differences in the time intervals of the investigations, and methods of microbial investigation, as well as difficulty of sampling microorganisms from the fallopian tube.55
Multiple organisms that usually colonize the lower genital tract were isolated from the normally sterile upper tract, and most infections were polymicrobial. These organisms included Gardnerella vaginalis, Escherichia coli, Haemophilus influenzae, group B beta-hemolytic streptococci, nonhemolytic streptococci, Prevotella bivia, Bacteroides species, Peptostreptococcus species, Mycoplasma hominis, and Ureaplasma urealyticum.
Salpingitis is believed to be an ascending infection that results from the direct canalicular spread of organisms from the endocervix to the endometrium and then the fallopian tube mucosa. According to Stamm et al and Platt et al, 10-40% of women not treated for gonococcal or chlamydial cervicitis develop clinical symptoms of acute salpingitis.56, 57
Four factors are thought to contribute to the ascent of these microorganisms.
Cervical and uterine instrumentation during intrauterine device (IUD) insertion, endometrial biopsy, and dilation and curettage (D&C) bypassing of the cervical mechanical barrier
Hormonal changes during menses and menstruation causing cervical alterations leading to a loss of the mechanical barrier including the bacteriostatic cervical mucus
Retrograde menstruation favoring ascent to the fallopian tubes
Virulence factors of the microorganism itself
However, rarely, salpingitis can result from the noncanalicular spread of cervical infection, possibly through parametrial lymphatics,58 or by hematologic spread from other infection sites.
Clinical presentation and diagnosis
The clinical presentation of salpingitis is highly diverse, ranging from asymptomatic to severe pelvic pain to diffuse peritonitis to, rarely, life-threatening illness. Poor correlation exists between the number and intensity of symptoms and the severity of tubal inflammation. This is seen frequently with C trachomatis infection where asymptomatic women are found to have severe tubal disease during infertility workup.
Since the diagnosis is usually based on clinical criteria, a high false-positive rate and a high false-negative rate can occur. For this reason, the classic clinical triad of fever, elevated erythrocyte sedimentation rate (ESR), and adnexal tenderness or mass required for the diagnosis of acute salpingitis has been dropped, as this triad was observed in only 17% of laparoscopically proven cases.50
In 1986, Hagdu et al reported no statistically significant difference between the following clinical symptoms among women with laparoscopically diagnosed acute PID and those who were visually healthy: lower abdominal pain, vaginal discharge, irregular bleeding, urinary symptoms, vomiting, proctitis symptoms, and marked tenderness on bimanual examination. The only statistically significant objective differences were temperature greater than 38°C, palpable mass or swelling on bimanual examination, ESR greater than 15 mm/h, and abnormal vaginal discharge.59
A low threshold for diagnosing PID is recommended because the clinical diagnosis of acute salpingitis is imprecise, current evidence indicates that many cases go unrecognized, and significant potential exists for irreversible damage to the fallopian tubes and associated health consequences.
In 1997, the Centers for Disease Control and Prevention (CDC) established guidelines for the diagnosis of acute PID and the minimum clinical criteria for initiating treatment.
Minimum criteria for clinical diagnosis of PID
Empiric treatment should be initiated in sexually active young women and others at risk for STDs if all of the following minimal criteria are met and no other causes of the illness can be identified:
Lower abdominal tenderness
Bilateral adnexal tenderness
Cervical motion tenderness
Additional criteria useful in diagnosing PID
Because incorrect diagnosis and management might cause unnecessary morbidity, the following criteria should be used to increase the specificity of the diagnosis.
Oral temperature greater than 38.3°C
Abnormal cervical or vaginal discharge
Elevated ESR and/or C-reactive protein levels
Culture or nonculture evidence of cervical infection with N gonorrhoeae or C trachomatis
Histopathologic evidence of endometritis on endometrial biopsy
Tubo-ovarian abscess (TOA) or thickened fluid-filled tubes with or without free-fluid on ultrasonography or other imaging techniques
Patients can be treated as outpatients; however, according to the 1998 CDC guidelines, patients should be hospitalized in the following cases:45
Pregnancy (See Medscape’s Pregnancy ResourceCenter.)
Presence of TOA
Patients are noncompliant or cannot tolerate oral therapy
Symptoms are severe and include nausea, vomiting, and high fever
Response to outpatient regimen is inadequate
Uncertain diagnosis and surgical emergencies
Patients are immunodeficient
A history of operative or diagnostic procedures
Peritonitis in the upper quadrants
Presence of IUD
Outpatient regimens include the following:
Regimen A – Ofloxacin 400 mg PO bid for 14 d, plus metronidazole 500 mg PO bid for 14 d
Regimen B – Ceftriaxone 250 mg IM once, or cefoxitin 2 g IM once and probenecid 1 g PO once, or other third-generation cephalosporins, plus doxycycline 100 mg PO bid for 14 d
Inpatient regimens include the following:
Regimen A – Cefotetan 2 g IV q12h, or cefoxitin 2 g IV q6h, plus doxycycline 100 mg IV or PO q12h
Discontinue cefoxitin 24 hours after patient’s symptoms improve and continue doxycycline 100 mg PO bid for a total of 14 days. If TOA is present, add clindamycin or metronidazole for better anaerobic coverage.
Regimen B – Clindamycin 900 mg IV q8h, plus gentamicin loading dose 2 mg/kg IV or IM, then 1.5 mg/kg IV q8h
Single daily doses may be substituted.
Alternative IV regimens include the following:
Ofloxacin 400 mg IV q12h, plus metronidazole 500 mg IV q8h
Unasyn 3 g IV q6h, plus doxycycline 100 mg IV or PO q12h
Ciprofloxacin 200 mg IV q12h, plus doxycycline 100 mg PO or IV q12h, plus metronidazole 500 mg IV q8h
According to the PID Evaluation and Clinical Health Study (PEACH), no difference exists in the effectiveness of inpatient and outpatient treatment strategies for patients with mild-to-moderate PID in preventing infertility, ectopic pregnancy, chronic pelvic pain, recurrence, and a good quality of life. Patients with mild-to-moderate PID were characterized by the following: a history of pelvic discomfort for a period of 30 days or less, findings of pelvic organ tenderness on bimanual examination, leukorrhea and/or mucopurulent cervicitis, and/or untreated, but documented, gonococcal or chlamydial cervicitis.60
Before antibiotics were available, mortality from acute salpingitis was about 1%. However, the mortality rate is much higher in cases complicated by ruptured TOA and in ectopic pregnancies.
Long-term sequelae include chronic pelvic pain, TOA, hydrosalpinx, tubal infertility, and ectopic pregnancy.
Chronic pelvic pain
The likelihood that a patient with acute salpingitis will develop chronic pelvic pain (20%) is 4 times that of patients without a pelvic infection (5%). The pain can be caused by resultant pelvic adhesions, TOA, or hydrosalpinx. Laparoscopy can be considered in these patients to establish the cause of the pain and rule out other causes, like endometriosis.
TOA is one of the major and serious complications of acute salpingitis and occurs in up to 15% of women with PID. Of women with a TOA, 33% require hospitalization.61 TOA is unilateral in 25-50% of cases. It forms as a consequence of acute salpingitis with pus collection within an anatomic space created by adherence of adjacent structures involving the fallopian tubes, ovaries, uterus, and sometimes the intestines, and, as such, is more precisely defined as a tubo-ovarian complex, while an abscess is a collection of pus in a newly created space.7 Clinically, however, these 2 conditions are managed the same way.
The formation of an abscess in relation to PID increases morbidity and the risk of treatment failure and subsequent operative intervention.62 Today, despite modern medical and operative management, mortality from ruptured TOA is 5-10%, mostly as a result of developing acute respiratory distress syndrome (ARDS).63
Using a rat model, Cox et al demonstrated that N gonorrhoeae and C trachomatis alone did not produce abscesses; however, when combined with facultative or anaerobic bacteria, synergism with abscess formation was noted frequently. This finding supports the hypothesis that N gonorrhoeae and C trachomatis initiate the infection and then aerobic and anaerobic bacteria act synergistically to produce abscesses. In addition, microorganisms, which were not inoculated, were recruited into the infectious process, gaining access to the peritoneal cavity via the lower genital tract or from transmucosal migration from the intestinal flora.64
The risk factors for the development of a TOA from PID have not been clearly defined, and a relation to IUD use has been difficult to evaluate. Landers et al found no statistical difference between the incidence of unilateral TOA in women with IUDs and those without IUDs.65
Although most TOAs develop from PID, several case reports exist of rare TOA formation not related to PID.
Canas et al reported TOA in a 12-year-old after total abdominal hysterectomy for cervical dysplasia, challenging the classic pathogenesis of TOA.66 Cases also exist of bilateral TOA that developed 50 days after a thermal ablation,67 after vaginal hysterectomy, and after colonic vaginoplasty for high cloacal anomaly in a 13-year-old girl.
Few cases of TOA were reported as resulting directly or indirectly following transvaginal ultrasonographic-guided oocyte retrieval for IVF and transcervical embryo transfer,68, 69 some suggesting that reactivation of latent pelvic infection due to a previous PID was the possible route of infection.
Cases have been reported of pelvic abscesses caused by Enterobius vermicularis, 70 Pasteurella multocida (which occurs most commonly following an animal bite wound or cat scratch),71 and Edwardsiella tarda infections (which have been reported in association with pet reptiles).72
Pompeo et al presented a case of unilateral chronic TOA secondary to ruptured colonic diverticulum presenting as a brain abscess.73
Clinical presentation and diagnosis of TOA
Typically, patients with an abscess present with acute pelvic pain, fever, and an adnexal mass, although the pelvic pain may be chronic. Patients may also report nausea, vomiting, a change in bowel habits, and vaginal discharge. Fever and leukocytosis may be absent. This clinical picture is not typically different from a patient diagnosed with PID alone. However, in severe cases, the patient can present with obstruction of the ureter and hydronephrosis,74 intestinal obstruction, or sciatic pain.75
Ultrasonography is helpful in identifying the adnexal mass and its size and characteristics. Typically, a TOA appears elongated, sausagelike, multiloculated, with thick borders that contain turbid fluid, and with abundant flow seen from the borders and the septa, with reduced resistance to flow on color Doppler.76
On CT scan, the most common appearance of TOA is that of a somewhat tubular septated cystic pelvic mass with uniform wall thickness and with loss of fat planes between the mass and the adjacent pelvic organs.77
MRI is an excellent radiologic modality in defining tissues and distinguishing between ovarian and tubal lesions, but it is also more expensive.
In cases of suspected ruptured TOA, culdocentesis can be a valuable diagnostic technique with 70% yield of purulent material.78
Management and outcome of intact TOA
An initial conservative antimicrobial approach to the management of the unruptured TOA is appropriate if the antimicrobial agents used can penetrate abscesses, remain active within the abscess environment, and are active against the major pathogens in TOA, which are predominantly anaerobes, including the resistant gram-negative anaerobes such as Bacteroides fragilis and Prevotella bivius. Clindamycin penetrates neutrophils that facilitate its passage inside the abscess and the stability of clindamycin within the microenvironment of the abscess has been proven. Adding an aminoglycoside completes the gram-negative coverage. This combination is considered the standard treatment of TOA. However, clindamycin does not cover Enterococcus species and, therefore, ampicillin should be added to that combination whenever Enterococcus is suspected. Metronidazole is an acceptable alternative to clindamycin.7
Landers et al demonstrated that single-agent, broad-spectrum antibiotics, such as cefoxitin, in conjunction with doxycycline, have efficacy that is equivalent to that of clindamycin-containing regimens.65 The overall medical treatment success rate of 75% suggests that conservative treatment of TOAs is warranted.79
The CDC STD Treatment Guidelines published in 2002 do not specify any particular treatment of TOA, but rather use the same parental regimen A and B as for PID. However, once the parental treatment is discontinued, the CDC suggest using clindamycin or metronidazole with doxycycline orally instead of doxycycline alone in regimen A and clindamycin orally instead of doxycycline in regimen B for better anaerobic coverage.80
If the patient does not begin to show a response within a reasonable amount of time, usually 48-72 hours, surgical intervention should be considered. Acute rupture is an indication for immediate operation. Once operation is undertaken, a conservative approach with unilateral adnexectomy for one-side TOA is appropriate if future fertility or hormone production is desired.65 Similarly, drainage of the abscess by either percutaneous drainage or a colpotomy incision may preserve the patient’s fertility.
Posterior colpotomy is preserved for abscesses in the cul-de-sac. The 3 requirements for colpotomy drainage63 are as follows:
Abscess must be in the midline.
Abscess should be adherent to the peritoneum of the cul-de-sac and dissect into the rectovaginal septum to ensure extraperitoneal drainage of pus.
Abscess should be cystic or fluctuant for adequate drainage.
Cases that do not meet the above criteria can be managed by percutaneous drainage or laparotomy.
Percutaneous aspiration or drainage of a TOA under ultrasonographic or CT guidance can be accomplished either transvaginally or transabdominally. In a series of 35 pelvic abscesses that resulted from PID, Worthen and Gunning demonstrated a success rate of 94% by aspiration drainage of 26 abscesses ranging from 2-11 cm in size, while catheter drainage of 9 abscesses ranging from 7.4-14 cm yielded only a 77% success rate.81 In a retrospective study of 27 pelvic abscesses, Corsi et al demonstrated a more than 90% success rate of transvaginal ultrasonographic-guided aspiration of the pelvic abscess while the patient was on broad-spectrum intravenous antibiotics.82 The perceived adequacy of drainage was correlated with lack of abscess septation. However, these studies were not randomized and were underpowered; larger studies need to be performed to claim an advantage of one method over the other, and long-term follow up is needed to assess the effect of such treatment on the rate of ectopic pregnancy, fertility, recurrence, and chronic pelvic pain.
Perez-Medina et al randomly distributed 40 women into 2 groups. Both groups received clindamycin and gentamicin, but in the study group, early transvaginal drainage of the abscess was performed. Both short-term (48-72 h) and medium-term (4 wk) responses to the treatment were evaluated. In 90% of the study group, a favorable short-term response was reported in terms of a decrease in leukocytosis, C-reactive protein, temperature, and size of the abscess evaluated sonographically, whereas only 65% in the control group responded to the same degree. Moreover, the average length of hospitalization was 3.9 days in the study group versus 9.1 days in the control group. In the medium-term follow-up, 1 patient in the study group and 3 in the control group had persistent adnexal mass on transvaginal sonography but no complications were present in both groups.83 As mentioned above, long-term follow-up is needed to assess the rate of recurrence, fertility, and ectopic pregnancy.
Definitive surgical management by exploratory laparotomy with conservative adnexal surgery is indicated in failed cases when either the abscess does not resolve or the patient does not improve clinically. To decrease the risk of complications, if possible, surgery should be delayed until after the infection has been quiescent and radiologic evidence of complete absorption of the inflammatory exudates surrounding the focus of infection is present. Ideally, the patient should have a normal ESR, WBC count, and hematocrit level and a relatively nontender pelvis, which usually takes about 2-3 months. However, when the patient on antibiotics does not improve clinically, surgery should be performed, and in this setting, the risk of complications, including bowel and bladder injuries, is higher.63
Whenever an abscess is drained, the content should be collected for aerobic and anaerobic cultures for identification of the microorganisms and their sensitivity to antibiotics.
Management and outcome of ruptured TOA
TOAs can rupture spontaneously into the rectum, sigmoid colon, bladder, or peritoneal space, but almost never into an intact vagina. Rupture can also result from accidental trauma or during bimanual examination.
The major symptom of a ruptured TOA is an acutely worsening pelvic pain that is so severe that the patient can usually precisely identify the time and location it occurred. On physical examination, the patient may appear critically ill with tachycardia, fever, distended abdomen, absent bowel sounds, signs of generalized peritonitis, muscle rigidity, shifting dullness, and direct and rebound tenderness. A pelvic mass is detected 50% of the time. Shock can develop while the patient is under observation due to accumulation of fluids in peripheral tissues and failure of compensatory vasoconstrictor mechanisms. The patient may be afebrile, and leukocytosis can be absent. Severe leukopenia is an ominous sign.63
A ruptured TOA is a surgical emergency because any delay in operative management increases mortality risk due to septic peritonitis and shock resulting from systemic absorption of bacterial endotoxins and significant third spacing into the peritoneal cavity through inflamed tissues. Speed is of the essence; the preoperative time should be reduced, and the operation should be performed in the fastest way possible.
Surgical treatment of TOA
Preoperative preparation for TOA may include the following:
A Swan-Ganz catheter may be necessary for hemodynamic monitoring and fluid resuscitation using crystalloid and partial colloid solutions to avoid fluid overload.
Blood products should be available, and if the patient is anemic, a transfusion should be considered prior to surgery.
Adequate correction of metabolic acidosis and electrolytes imbalance
Adequate respiratory support
Intravenous broad-spectrum antibiotics
Intestinal tube to decompress dilated intestines
The ideal operation includes removal of pus, abscess, uterus, tubes, and ovaries. If the abscess involves only 1 adnexa, then a unilateral salpingo-oophorectomy can be attempted in a young patient, although leaving the uterus increases the risk of recurrence in the unaffected tube. In these cases, hysterectomy should be considered—usually a supracervical hysterectomy since it is achieved faster. Copious irrigation with warm saline prior to closure of the incision removes and dilutes any remaining bacteria in the peritoneum.
The postoperative course can be complicated by intestinal obstruction or fistulas, pelvic and abdominal abscesses, separation or dehiscence of the incision, septic shock, disseminated intravascular coagulation (DIC), pulmonary embolus, and ARDS.
Pyosalpinx and hydrosalpinx
Pyosalpinx is defined as pus in the fallopian tube, which usually results from acute salpingitis. If the infection is severe and spreads to the adjacent structures, it forms a TOA. On the other hand, if the fimbrial end becomes occluded, the infection is contained within the tube and it forms a pyosalpinx. Grossly, the tube appears distended and is filled with pus. Microscopically, the tubal wall is thickened and infiltrated by acute and chronic inflammatory cells. The plicae of the tube are swollen and edematous.
Hydrosalpinx is a collection of watery sterile fluid inside the fallopian tube. It results from tubal obstruction as an end stage of pyosalpinx. Grossly, it appears as a dilated tube with a thin wall and is filled with clear, colorless, watery fluid, which results from proteolysis of neutrophils and debris. The external surface may have adhesions. Microscopically, the thin and dilated tubes have flattened epithelium, but both ciliated and secretory cells can be recognized.
On ultrasonography, hydrosalpinx appear as elongated, sausagelike, cystic lesions with thin borders that contain clear fluid with or without septa. The addition of color Doppler flow helps in distinguishing hydrosalpinges from ovarian lesions by demonstrating flow from the borders (and usually not from the thin septa), with a higher resistance than ovarian flow (mean resistive index of 0.752 vs 0.55), while in TOAs the resistance is much lower (mean resistive index 0.448) secondary to the inflammation.76
The major clinical significance of a hydrosalpinx is its adverse effect on fertility. This effect is thought to be due to more than just the destruction and occlusion of the fallopian tube. The presence of a hydrosalpinx is associated with up to a 50% reduced implantation and pregnancy rate after IVF.84 This reduction is thought to result from the presence of embryo toxin in the hydrosalpinx fluid. These toxins are yet to be identified. Therefore, excising the hydrosalpinx prior to performing IVF is recommended.
In a Cochrane database systematic review, Johnson et al concluded that laparoscopic salpingectomy should be considered for all women with hydrosalpinges prior to IVF treatment, although further evaluation is needed and randomized trials are required to assess other surgical options for hydrosalpinx, such as salpingostomy, tubal occlusion, or needle drainage of a hydrosalpinx at oocyte retrieval.85
A hydrosalpinx, although sterile, can be reinfected leading to a pyosalpinx. Nikolic et al published a case of the development of a pyosalpinx from a preexisting hydrosalpinx after uterine artery embolization for leiomyomata.86
Salpingitis Isthmica Nodosa
Salpingitis isthmica nodosa (SIN) or tubal diverticulum is an acquired pathologic condition that results from the direct invasion of the muscularis layer by the endosalpinx in the isthmic portion of the fallopian tube for varying distances between the lumen and the serosa.
First diagnosed in 1951 on hysterosalpingography, SIN affects about 5% of young women, with a mean age of 26 years, and is more common in the Jamaican population. It is bilateral in about 85% of cases. The etiology of SIN is unknown, but it is thought to be an inflammatory condition of the fallopian tubes most likely acquired during the reproductive years as a consequence of an infection. However, a direct association with an infective process has yet to be proven. Patients usually have histologic evidence of previous salpingitis, may have high serum chlamydial antibody titers, and may have the presence of the major outer membrane protein of C trachomatis in the involved tube.87 Creasy et al found that 89% of the tubes involved with SIN had evidence of an associated inflammation on historic, radiologic, surgical, or histologic grounds. They concluded that SIN is a condition that either is a direct consequence of an infection or predisposes the patient to subsequentinfections.88
Grossly, localized nodular thickening or swelling of the isthmus can be identified during laparoscopy. This swelling represents secondary hyperplasia and hypertrophy of the myosalpinx surrounding the diverticula, which microscopically are up to 2 mm in size and represent hypertrophied tubal mucosal glands penetrating the myosalpinx.
On hysterosalpingogram, the fallopian tubes appear normal in size and position; however, numerous small round luminal outpouchings of contrast material are seen in the isthmic portion. These represent the diverticula protruding from the lumen into the myosalpinx.
The clinical significance of SIN relies on its strong association with infertility and ectopic pregnancy. In at least one series by Green et al, SIN was found in 50% of fallopian tubes removed from patients with ectopic pregnancy as compared with only 5% of the control group.89
Although the exact mechanism is not known, SIN is believed to contribute to infertility and ectopic pregnancies by affecting the normal transportation function of the tube and not by mechanical obstruction; most tubal pregnancies implant distally to the affected segment.
Surgical correction of SIN by tubocornual anastomosis (TCA) or by transcervical recanalization (TCR) of the tubes has been suggested. Those who advocate TCA stress the importance of resection of the diseased proximal oviduct, not simply the restoration of tubal patency, as patency does not restore the function of the involved tube. Intrauterine pregnancy (IUP) rate after TCA (55%) uniformly exceeds the IUP rate after cannulation (28%), reflecting the inability of cannulation to correct myosalpingeal disease.90
However, the relevance of tubal surgery in this era of IVF and embryo transfer is highly debated and depends on the couple’s resources and preferences.
Endosalpingiosis, first described by Sampson, refers to the presence of tubal epithelium outside the fallopian tubes, most commonly involving the peritoneal surface of the uterus, fallopian tubes, ovaries, or cul-de-sac.91 It is most often an incidental finding, affecting about 8% of women.92
The pathogenesis of endosalpingiosis is similar to that of endometriosis. The different theories of endometriosis also apply to endosalpingiosis and include the metaplasia theory, the implantation or invasion theory after surgery or manipulation, and the metastatic theory. The first theory implies that the adult peritoneum retains the potential to differentiate into various types of epithelium, and metaplasia may be induced by different stimuli, such as hormones, inflammation, and menstruation.
Diagnosis is made histologically by the presence of tubelike epithelium containing 3 types of cells: ciliated columnar cells, secretory cells, and peg cells. Varying degrees of cellular atypia rarely occur in endosalpingiosis, so-called atypical endosalpingiosis, which can occur in cases of tumorlike cystic endosalpingiosis and need to be differentiated from borderline tumors and well-differentiated adenocarcinoma.93, 94 Most patients in whom diagnosis is made are asymptomatic, and the finding is purely incidental. However, in others, the diagnosis is made during laparoscopic workup of infertility or pelvic pain. Whether endosalpingiosis causes pelvic pain is unclear.95, 96, 97
Redondo et al reported a case of cutaneous umbilical endosalpingiosis with severe abdominal pain that resolved after local resection,98 while others reported painless cutaneous umbilical implants.99
Ectopic pregnancy is the leading cause of pregnancy-related death during the first trimester. In 1992, ectopic pregnancies accounted for approximately 2% of reported pregnancies, and ectopic pregnancy-related deaths accounted for 9% of all pregnancy-related deaths. From 1970-1992, the incidence of ectopic pregnancy increased from 4.5 per 1000 to 19.7 per 1000 reported pregnancies. The increased occurrence of ectopic pregnancy in the United States is consistent with the trend in increased prevalence of risk factors for ectopic pregnancy; however, improved early diagnostic techniques also contribute to the apparent increased incidence.100
The major cause of ectopic pregnancy is acute salpingitis, accounting for 50% of cases. In 40% of cases, the cause is unknown, but physiologic factors, like hormonal variation, have been a speculated etiology. The previously theorized transmigration of the ovum from the contralateral ovary has been widely disputed.
The remaining causes can be attributed to the following:7
Progestin-only pills or progesterone-releasing IUD, which can alter the tubal contractility and delay the fertilized egg from reaching the endometrial cavity
Clomiphene citrate– or human menopausal gonadotrophins–induced ovulation with the release of multiple eggs, increasing the likelihood of a fertilized egg to be trapped within the tube
Pelvic and tubal surgery including failed tubal sterilization
Salpingitis isthmica nodosa (SIN)
History of in utero exposure to diethylstilbestrol (DES)
Cigarette smoking, being an independent and dose-related effect
Abnormality in embryonic development, with aneuploidy found in one third of ectopic gestations, excluding inherited genetic abnormalities because no increase is apparent among first-degree relatives
In 1970, Breen showed that more than 97% of ectopic pregnancies occur in the fallopian tube, with 81% in the ampullary region, 12% in the isthmus, and 5% in the fimbrial area.101
Acute salpingitis destroys the microscopic and macroscopic structure of the fallopian tube, leading to the fusion of the plicae. These destroyed folds allow the sperm to pass through but prevent the passage of the larger morula. Intra-abdominal and peritubal adhesions, occurring as a consequence of this infection, may also be a major factor in distorting the tubal architecture and motility. Using ligase chain reaction (LCR), Noguchi et al have detected C trachomatis infection using DNA extracted from paraffin-embedded tubal tissues.102
Pelvic adhesions due to previous abdominal surgeries also interfere with the motility of the tube. However, no clear association of ectopic pregnancies and endometriosis with or without adhesions exists.
SIN, as previously described, was found in 50% of tubal segments resected in ectopic pregnancy cases. Although the exact mechanism is not known, SIN is believed to contribute to infertility and ectopic pregnancies by affecting the normal transportation function of the tube and not by mechanical obstruction; most tubal pregnancies implant distally to the affected segment.
Tubal surgery increases the risk of ectopic pregnancy, but that risk depends on the indication for the surgery. Salpingoplasty or salpingostomy for tubal disease have higher risk of ectopic pregnancy (15-25%) than reversal of sterilization procedures (4%) because the tube has not been damaged by infection.7
Infertility and Tubal Factor
In 2002, 12% of women aged 15-44 (7.3 million women) had impaired fecundity, which is a physical difficulty getting pregnant or carrying a baby to term. This number has increased about 2% from the levels seen in 1988 and 1995. In 2002, about 15% of married women (an estimated 4.3 million) had impaired fecundity. Additionally, 7.4% of married women (about 2.1 million) were infertile, about the same level as seen in 1995, but representing a significant decline from the prevalence of 8.4% in 1982.103
Tubal factors are responsible for 25-30% of infertility cases, with acute salpingitis being the most common cause, representing more than half of the cases. Salpingitis partly contributes to the increased number of infertility cases as the occurrence has increased over the past 2 decades. Estimates show that after one episode of PID, an 11% risk of infertility is present. This risk increases to 23% after 2 episodes of PID and is as high as 54% after 3 episodes.104, 90, 105
Tubal obstruction can involve the distal, proximal, or entire tubal segment and can be partial or complete. The degree of obstruction is best diagnosed using hysterosalpingogram (HSG). Some experts advocate using laparoscopy, in addition to HSG, to establish the extent of the disease. Laparoscopy determines the size of hydrosalpinx and the extent of pelvic adhesions, if present. The extent of the disease, its location, and the amount of remaining healthy tubal segment determines the prognosis of successful pregnancy following tubal reconstructive surgery and whether IVF will provide a better outcome. If hydrosalpinges are present, excising the diseased tubes prior to performing IVF would be best.
Distal tubal obstruction is much more common (70%) than proximal obstruction. It can be caused by hydrosalpinges, pelvic adhesions, or fusion of the fimbriae. According to Schlaff et al, the presence of rugal pattern on HSG, the absence or presence of small hydrosalpinges less than 15 mm in diameter, the absence of significant pelvic adhesions, and the presence of identifiable fimbriae with patent ostium during laparoscopy were all associated with good prognosis following tubal reconstructive surgery106, 107 About 80% of those women with mild tubal disease conceived. Patients with moderate and more severe disease had a much worse prognosis of achieving uterine pregnancy, and the risk of ectopic pregnancy was as high as 30% in some series.108
Proximal tubal obstruction is most commonly caused by infection, endometriosis, myomas, salpingitis isthmica nodosa (SIN), or dried mucus. It can be misdiagnosed during HSG due to a spasm of the intramural segment when the dye is injected. This can be avoided by slowing the speed of injection, or, if this fails, laparoscopy with chromotubation is warranted. Laparoscopy is also beneficial in examining the distal portion of the tube in case of proximal obstruction. The extent of the disease determines the success of microsurgical tubocornual reanastomosis.
Donnez and Casanas-Roux found that pregnancy was achieved in 55% of the women when the interstitial portion of the tube was not damaged during microsurgery and less than 1.5 cm of the occluded tube needed to be excised. Alternatively, selective HSG and proximal tubal canalization may be used to open the tubes.108 This can be performed using fluoroscopy or hysteroscopy under local sedation where a catheter and guidewire system are used to clear proximal tubal obstructions. The recanalization procedure is successfully completed in most patients with patency achieved in 60-85% of patients and resulting in pregnancy in about 30%.
Isolated Tubal Torsion
Isolated tubal torsion with ovarian sparing is an uncommon cause of acute lower abdominal pain, and primary case reports have been published in the medical literature. The presumed incidence of isolated tubal torsion is about 1 in 1.5 million. It occurs at all ages, although most frequently during reproductive age, in normal as well as diseased tubes, in pregnancy, and even after tubal sterilization. Rarely, it can be bilateral.109
The etiology of isolated tubal torsion has been subdivided into intrinsic and extrinsic factors.110 Intrinsic factors include hydrosalpinx, tubal tumor, congenital abnormalities, and prior surgery (including tubal ligation). The extrinsic factors include ovarian and paratubal masses, trauma, adhesions, pelvic congestion, pregnancy, and sudden body movements. These factors contribute to the torsion by providing a point of reference around which the tube can twist.111, 112
Bernadus et al suggested that the process begins with the mechanical blockage of the adnexal veins and lymphatic vessels by 1 of the above factors, and this obstruction causes pelvic congestion and local edema, with subsequent enlargement of the adnexa, which, in turn, induces partial or complete torsion. Furthermore, the mechanical blockage of the distal part of the fallopian tubes, together with the normal secretion of the fallopian tube glands, can cause a hydrosalpinx, a risk factor by itself for torsion.113, 110, 114
Clinically, isolated tubal torsion presents as a convulsive pelvic pain that worsens with time, with or without peritoneal signs; the pain can radiate to the groin, flank, or thigh and is accompanied by nausea, vomiting, and occasionally urinary symptoms. On bimanual examination, adnexal tenderness, with or without a mass, and, at times, cervical motion tenderness are present. Because of the lack of specific signs and symptoms, and because laboratory values are usually nonspecific, isolated tubal torsion is often missed.115 Diagnosis is mainly made using laparoscopy.
In a few published cases, color Doppler ultrasonography was helpful in making the preoperative diagnosis.116 These reports noted a dilated fallopian tube with a hyperechoic wall, a folded configuration with a focus of echogenicity protruding into the lumen, possibly related to a wrinkled fallopian tube epithelium. Sometimes, a spiral appearance related to the pattern of papillary projections and tapering of the tube as it approaches the uterine cornua and possible point of torsion were seen. Color Doppler ultrasonography can demonstrate normal ovarian blood flow and high-impedance flow with reversed diastolic or absent flow in the wall on the dilated tube or mass. These findings become more specific once added to the clinical picture of acute adnexal pain, especially with a history of prior tubal ligation.111
Detection and detorsion of a torsed adnexa by laparoscopy has been recommended as the treatment of choice for patients of reproductive age in the attempt to preserve the tube and fertility. Early diagnosis by laparoscopy increases the chances of revascularization of the torsed ischemic adnexa.
Paratubal cysts are usually asymptomatic; they commonly occur in women aged 30-40 years and are usually discovered incidentally during surgery for other gynecologic reasons. Together with paraovarian cysts, they constitute 10% of all adnexal masses. They are often multiple and small but can vary in size from 0.5 cm to more than 20 cm and can be mistaken for an ovarian mass. When the cysts are in proximity to the ovary, they are called paraovarian cysts. Hydatid cysts of Morgagni are paratubal cysts that are pedunculated and in close contact with the fimbriated end of the fallopian tube.
Paratubal cysts are usually translucent, unilocular, filled with clear serous fluid, and lined by flattened cuboidal epithelium. They are most commonly remnants of the paramesonephric duct but may also be of mesonephric or mesothelial origin.
Most paratubal cysts are asymptomatic, but they may rarely give rise to clinical problems due to enlargement or torsion. In one series of 338 white female patients aged 4-14 years with right lower pelvic pain, laparotomy revealed acute appendicitis in 283 cases, while 44 patients had acute appendicitis plus a coincidental paratubal cyst. Most of these cysts were smaller than 1 cm in diameter. However, 2 additional patients had torsion of a large paratubal cyst, while 5 had a ruptured corpus luteum.117
During pregnancy, paratubal cysts can grow rapidly causing torsion. Management is simple excision.
Rarely, malignant changes occur within the cyst, most of which are serous borderline tumors of endometrioid type with low malignant potential. However, few cases of serous papillary cystadenocarcinoma with capsular invasion, as well as transitional cell carcinoma, have been documented.118, 119, 120, 121 Most of these cases arose from cysts larger than 5 cm in diameter and had internal papillary projections not noted on external examination of the cyst. For this reason, some experts caution again cyst aspiration as such practice can miss and potentially disseminate a malignant disease.122
Preoperative diagnosis is difficult, as ultrasonography cannot differentiate paratubal cysts in close proximity to the ovary from an ovarian cyst.123
During surgery for large paratubal cysts, the fallopian tube is often found to be stretched over the large mass. If technically possible, the tube should not be excised, as it will return to normal shape.
Benign tubal tumors
Leiomyomas: Fewer than 100 cases of leiomyomas of the fallopian tube have been described in the literature, largely because they are underreported. Mainly asymptomatic and discovered incidentally, tubal leiomyomas may be single or multiple and may vary in size, ranging from microscopic to more than 15 cm in diameter. Histologically, they are similar to the more common uterine myomas and may be subserosal, submucosal, or interstitial. They originate from the smooth muscles of the tube, broad ligament, or even the blood vessels. Although asymptomatic, tubal leiomyomas can cause obstruction of the fallopian tube resulting in an ectopic pregnancy, although this is rare.124 The tubal leiomyomas can also undergo acute degeneration resulting in severe pelvic pain similar to uterine myomas. Management is by excision.
Lipomas: Although lipomas are among the most common benign soft tissue tumors, fallopian tube lipomas are underreported, typically because they are unrecognized.125 Lipomas can occur in association with mature cystic teratomas of the ovary, which are the most common fat-containing ovarian neoplasm.126
Adenomatoid tumors: Adenomatoid tumors of the fallopian tube are common and often associated with leiomyomas and adenomyosis of the uterus. They appear as small subserosal nodules 1-2 cm in size, gray-white in color, and circumscribed. They are formed of a combination of 2 tumor types, adenoid and angiomatoid, can be solid or cystic, and are of mesothelial origin. Diagnosis is made histologically, as they are difficult to differentiate from leiomyomas. These tumors are typically asymptomatic and discovered incidentally.