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Pregnancy tests using animals

Pregnancy tests using animals, also known as biological assays for detecting human chorionic gonadotropin (hCG) in urine, were a cornerstone of prenatal diagnostics from the early 20th century until the 1960s, relying on the physiological responses of various species to injected samples from potentially pregnant individuals.^[1] These tests emerged following the discovery of hCG as a pregnancy-specific hormone in the 1920s, with the first widely adopted method being the Aschheim-Zondek test developed in 1927 by Selmar Aschheim and Bernhard Zondek, which involved injecting urine into immature female mice and examining ovarian changes such as the formation of corpora lutea after approximately 100 hours to confirm pregnancy, achieving accuracies of 82.5% to 99.5%.^[1] In 1931, Maurice Harold Friedman introduced the Friedman test using female rabbits, where a single intravenous injection of urine induced ovulation detectable within 48 hours via surgical examination or autopsy, offering similar high accuracy and becoming a standard in clinical laboratories due to its reliability.^[1] Further innovations in the 1940s expanded options with less invasive procedures; the Hogben test, devised by Lancelot Hogben, utilized the African clawed frog (Xenopus laevis), injecting urine subcutaneously and observing for egg deposition within 2 to 12 hours as a positive indicator, with the advantage of reusing the frogs without sacrifice.^[1] Similarly, the 1947 Galli-Mainini test employed male South American toads (Bufo arenarum), where urine injection into the lymphatic sac prompted spermiation (sperm release) within 3 to 5 hours, detectable by microscopic examination of urine, minimizing animal harm and allowing rapid results.^[1] By the mid-20th century, these animal-based assays were performed in specialized labs worldwide, processing thousands of tests annually and playing a pivotal role in obstetrics, though they raised ethical concerns over animal welfare due to frequent sacrifices in methods like the Aschheim-Zondek and Friedman tests.^[1] ^[2] Their decline began in the 1960s with the advent of immunological and chemical detection kits, which eliminated the need for live animals and enabled at-home testing by the 1970s, rendering bioassays obsolete by the 1980s.^[1]

Background

Historical Context

Before the development of reliable biological assays in the early 20th century, attempts to diagnose pregnancy relied on rudimentary and often unscientific methods. In ancient Egypt around 1350 BCE, a common practice involved urinating on wheat and barley seeds; if the seeds sprouted, it was interpreted as a positive sign of pregnancy, though this method lacked scientific validation and had low accuracy.^[1] Similar non-empirical approaches persisted through the Middle Ages and into the 19th century, including visual inspections of urine for color or sediment and provocative tests like administering sweet drinks to observe reactions.^[1] By the early 1900s, chemical-based efforts emerged, such as Emil Abderhalden's 1912 serum reaction test, which aimed to detect pregnancy-specific proteins in blood through enzymatic breakdown but proved unreliable due to frequent false positives and lack of specificity.^[3] The breakthrough in pregnancy testing came in the 1920s amid growing understanding of reproductive hormones. In 1927, German researchers Selmar Aschheim and Bernhard Zondek discovered that urine from pregnant women contained a substance—initially termed the anterior pituitary-like hormone, later identified as human chorionic gonadotropin (hCG)—that induced specific physiological responses in animals, laying the foundation for the first dependable diagnostic method.^[1] This insight shifted pregnancy detection from speculative techniques to biologically grounded assays, enabling the introduction of the Aschheim-Zondek test in 1927, which used immature female mice to detect hCG.^[4] Subsequent innovations expanded the use of animal models. In 1931, Maurice Friedman developed a variant using rabbits, which offered faster results; this was followed by Lancelot Hogben's 1930 test employing the African clawed frog (Xenopus laevis) for its sensitivity to hCG-induced ovulation.^[1] By 1947, Carlos Galli-Mainini introduced a test with male South American toads, which responded by producing sperm, further simplifying the process.^[5] These methods reached their zenith in the 1940s and 1950s, with millions of tests conducted annually worldwide across laboratories, achieving accuracies of 82.5% to 99.5% and becoming a standard tool in clinical practice.^[1] The advent of these animal-based tests had profound social implications by allowing early pregnancy confirmation as soon as one to two weeks after a missed period, far surpassing the previous reliance on delayed physical symptoms or invasive pelvic examinations.^[6] This timeliness facilitated better prenatal care planning, reduced uncertainty for women, and supported broader access to reproductive health services during a period when such diagnostics were transformative for family and medical decision-making.^[1]

Scientific Foundation

Human chorionic gonadotropin (hCG) is a glycoprotein hormone produced by trophoblast cells of the placenta shortly after implantation of the fertilized embryo, serving as a key marker of early pregnancy.^[7] Its primary role involves maintaining the corpus luteum to sustain progesterone production, thereby supporting the uterine lining and preventing menstruation.^[7] Structurally, hCG comprises two subunits: an alpha subunit shared with other glycoprotein hormones like luteinizing hormone (LH) and follicle-stimulating hormone (FSH), and a beta subunit unique to hCG that enables specific immunological and biological detection.^[7] In pregnancy, serum hCG levels rise rapidly, doubling approximately every 48 hours in the first weeks and peaking around 8-10 weeks of gestation at levels up to 100,000-200,000 IU/L before gradually declining.^[7] The biological mechanism underlying animal-based pregnancy tests relies on hCG's ability to mimic LH, binding to the same receptors (LHCGR) on gonadal cells across various species.^[8] This structural homology—particularly in the beta subunit, with about 80-85% similarity between hCG and LH—allows exogenous hCG from human urine to stimulate reproductive responses in injected animals, such as ovarian follicle maturation, ovulation in females, or spermatogenesis in males.^[8] In practice, this induces observable changes like corpora hemorrhagica formation or egg release, confirming hCG presence. Sensitivity to hCG varies by species due to differences in receptor affinity and metabolic clearance; mammals such as rodents and rabbits typically respond to lower doses (around 1-5 IU), while amphibians require higher thresholds (up to 200 IU or more) for equivalent responses.^[9] Animals were chosen for these tests based on their pronounced and reliable gonadal responses to hCG, which amplify subtle hormonal signals into macroscopic endpoints. Immature female rodents, for instance, develop ovarian hyperemia and follicle enlargement in response to low hCG doses, while mature female rabbits exhibit rapid ovulation within 24-48 hours, facilitating quicker assessments.^[2] Amphibians like the African clawed frog (Xenopus laevis) release eggs within 12 hours of injection, offering a non-lethal, reusable model despite lower sensitivity. These tests could reliably detect urinary hCG concentrations as low as 5-10 IU/L, corresponding to early pregnancy stages around implantation.^[7] To standardize results and enhance detectability, urine samples were often concentrated through evaporation to reduce volume and increase hCG density, or administered in fixed injection volumes (e.g., 0.5-5 mL subcutaneously or intravenously) to control dosage exposure.^[2] However, false positives could arise from ectopic hCG production unrelated to pregnancy, such as in gestational trophoblastic diseases or germ cell tumors, where elevated levels mimic pregnancy signals.^[7]

Aschheim-Zondek Test

Procedure

The Aschheim-Zondek test uses immature female mice, typically 3-5 weeks old and weighing 6-10 grams, as test subjects, with 3-5 mice required per test to ensure reliability.^[4]^[10] To perform the test, a urine sample from the woman is first tested for acidity and adjusted to a basic pH if necessary, with 1-2 drops of tricresol added as a preservative and the sample filtered if cloudy. Approximately 0.2-0.5 mL of urine is then injected subcutaneously into each mouse, administered twice daily for three consecutive days at different body sites, followed by a rest day on the fourth day.^[4]^[10] After approximately 100 hours from the first injection (totaling about 5 days), the mice are euthanized humanely, dissected, and their ovaries examined macroscopically and microscopically for changes indicative of human chorionic gonadotropin (hCG) exposure.^[1]^[4] A positive result is indicated by ovarian hyperemia (enlargement to 2-3 times normal size with red hemorrhagic spots), formation of corpora lutea, or mature follicles; the uterus may also show enlargement or specific vaginal cell changes (e.g., "Schollenstadium"). Absence of these ovarian changes, potentially with only uterine enlargement, indicates a negative result, though repeat testing is recommended if heat signs are present. The test was developed in 1927 by German researchers Selmar Aschheim and Bernhard Zondek and achieved approximately 98% accuracy in early clinical use.^[1]^[10]

Advantages and Limitations

The Aschheim-Zondek test provided significant advantages as one of the first reliable biological assays for pregnancy, offering high specificity for detecting hCG produced by placental tissue, with reported accuracy rates of 98-98.9% based on thousands of evaluations. It enabled early diagnosis from the fourth week of pregnancy and was also useful for identifying conditions like ectopic pregnancy, hydatidiform mole, chorioepithelioma, incomplete abortion, and certain testicular tumors, making it a foundational tool in endocrinology and obstetrics during the 1920s-1950s.^[1]^[4] However, the test had key limitations that limited its practicality. It was time-intensive, requiring up to 5 days for results, which delayed clinical decisions compared to later methods. The procedure involved euthanizing multiple mice per test, raising early ethical concerns about animal welfare and increasing operational costs due to the need for a steady supply of immature animals. False negatives (about 1-2%) could occur with very early pregnancies or interfering substances like certain medications (e.g., sleeping pills or painkillers), while false positives were rare but possible in non-pregnancy hCG-producing conditions. The complexity demanded skilled technicians for injections and dissections, restricting it to specialized laboratories, and it became obsolete by the 1960s with the rise of non-animal immunological tests.^[4]^[10]

Friedman Test

Procedure

The Friedman test utilizes sexually mature, non-pregnant female rabbits, typically post-partum or virgin adults weighing 2-3 kg, as test subjects.^[11] To perform the test, a sample of the woman's morning urine (concentrated, with fluid intake restricted to 6 oz from 4 p.m. the previous day) is collected, refrigerated, filtered to remove precipitates, acidified if alkaline, and warmed to body temperature. Approximately 4-10 mL of prepared urine is injected intravenously into the rabbit's marginal ear vein using a 23-gauge needle, often under light anesthesia. A single injection or up to three daily injections over two days may be used, depending on the variant.^[11]^[12] The rabbit is then maintained under observation for 24-48 hours post-injection. At the end of this period, the animal is anesthetized with ether, and the ovaries are surgically exposed or examined via autopsy to check for physiological changes.^[11] A positive result is indicated by the presence of ruptured or hemorrhagic ovarian follicles, fresh corpora lutea, or corpora hemorrhagica in the ovaries, which are triggered by human chorionic gonadotropin (hCG) in pregnant urine stimulating ovulation. The degree of reaction may be graded from 1+ to 4+ based on the extent of ovarian and uterine changes, such as congestion and swelling of the uterine horns. Absence of these changes indicates a negative result. Due to the need for invasive examination, the rabbit is typically sacrificed after the procedure.^[11] Developed in 1930 by American physiologist Maurice Harold Friedman and Maxwell Edward Lapham at the University of Pennsylvania, this test requires surgical tools, anesthesia, and microscopic or gross examination capabilities, and achieved high accuracy rates of 95-99% in clinical use for detecting pregnancy from the fourth week onward.^[12]^[13]

Advantages and Limitations

The Friedman test provided significant advantages over earlier methods like the Aschheim-Zondek test, primarily through its faster results and simplified protocol. Unlike the multi-day subcutaneous injections and extended observation (up to 100 hours) required for the Aschheim-Zondek mouse assay, the Friedman test delivered results within 24-48 hours via a single or few intravenous injections, facilitating quicker diagnoses in clinical settings. It demonstrated high sensitivity to hCG, reliably detecting pregnancies as early as 7-10 days after a missed period, with reported accuracy between 95% and 99% in large-scale evaluations during the 1930s-1950s. The test's specificity allowed differentiation of pregnancy from conditions like hydatidiform mole or chorionepithelioma, where excessive gonadotropins produced similar ovarian responses. Its adoption in laboratories worldwide made it a standard for prenatal confirmation until the 1960s, processing thousands of samples annually.^[11]^[13] However, the test had substantial limitations, most notably its ethical and practical drawbacks due to animal sacrifice. Each test required killing the rabbit via surgical exploration or autopsy to inspect the ovaries, leading to the consumption of tens of thousands of rabbits yearly and raising animal welfare concerns even in its era. The procedure demanded skilled personnel for intravenous injection and surgical examination, increasing operational complexity and cost compared to later non-invasive assays. False negatives could occur with dilute or improperly handled urine (e.g., if not concentrated or contaminated), while false positives were possible from non-pregnancy sources of gonadotropins, such as pituitary tumors, menopause, or certain urinary toxins that stressed the animal. Sensitivity was lower in very early pregnancy (before hCG exceeds 500 IU/L) or late stages when hormone levels fluctuate. Additionally, the test's reliance on live rabbits posed logistical challenges, including breeding, housing, and disposal, limiting its use in resource-poor areas. By the 1950s, less invasive alternatives like the Hogben and Galli-Mainini tests began supplanting it, highlighting its humane and efficiency shortcomings.^[11]^[14]

Hogben Test

Procedure

The Hogben test utilizes sexually mature female African clawed frogs (Xenopus laevis), typically 8-12 cm in length, as the test subjects.^[1] To perform the test, 0.5-1 mL of the woman's urine is injected subcutaneously into the dorsal lymph sac of the frog using a fine needle.^[1] The frog is then placed in a container of water to maintain hydration and left undisturbed for 2-12 hours.^[1] Following the incubation period, the water is examined for the presence of eggs. A positive result is indicated by the deposition of eggs, triggered by human chorionic gonadotropin (hCG) in pregnant urine inducing ovulation; absence of eggs indicates a negative result. The frog is reusable for multiple tests after a recovery period of several days.^[1] Developed in the 1940s by British zoologist Lancelot Hogben, this method requires basic equipment such as a syringe for injection and a container for observation, and demonstrates high accuracy, with reported rates of 93-99% in clinical use.^[1]

Advantages and Limitations

The Hogben test offered several advantages over earlier animal-based pregnancy diagnostics, particularly in its non-lethal nature and efficiency. Results could be obtained within 2-12 hours, faster than the Aschheim-Zondek test's 100 hours but comparable to the Friedman test's 48 hours, allowing for timely clinical decisions. Unlike mammalian tests that required sacrificing the animals for ovarian examination, the Hogben test allowed reuse of the frogs without harm, reducing ethical concerns, costs, and logistical needs for constant animal supply. The use of Xenopus laevis, which could be maintained in aquaria, made it practical for laboratories worldwide, and its specificity for hCG provided accuracy rates of 93-99% in studies, effective for detecting pregnancies from the second week onward when hCG exceeds 100 IU/L.^[1] However, the test had limitations that affected its reliability and practicality. It required specialized maintenance of live frogs, including controlled environments to prevent disease or stress, which could vary results if animals were unhealthy. False positives arose from cross-reactivity with luteinizing hormone (LH) in non-pregnant urine, such as during ovulation or in conditions like menopause, leading to specificity issues in 3-7% of cases. Sensitivity was lower in very early pregnancy (before 10-14 days post-missed period), with detection rates as low as 12% in the first week rising to 93% by the third. Operator interpretation of egg presence was subjective without standardization, and the need for fresh urine samples limited remote testing. By modern standards, the use of animals raises significant ethical concerns regarding welfare and potential stress from repeated injections.^[1] Historically, the test was widely adopted from the 1940s to the 1960s in Europe, North America, and South Africa, where Xenopus was readily available, processing thousands of samples annually in specialized labs and contributing to accessible prenatal care before immunological tests supplanted it.^[1]

Galli-Mainini Test

Procedure

The Galli-Mainini test utilizes adult male frogs, such as Rana pipiens, or toads, such as Bufo arenarum, measuring 5-10 cm in length as the test subjects. Originally developed using the South American toad Bufo arenarum, it was adapted to species like the North American frog Rana pipiens.^[15]^[1] To perform the test, a small volume of the woman's urine is injected subcutaneously into the dorsal lymph sac of the animal using a fine needle.^[15] The frog or toad is then placed in a moist container to maintain hydration and left undisturbed for 2-5 hours.^[15]^[16] Following the incubation period, a urine sample is collected from the amphibian by gentle bladder expression or via catheterization to avoid contamination. The sample is immediately examined under a light microscope at low magnification for the presence of spermatozoa, particularly motile forms in the sediment.^[15] A positive result is confirmed by the observation of sperm in the urine, triggered by human chorionic gonadotropin (hCG) in pregnant urine inducing spermiation; absence of sperm indicates a negative result. The test animal is reusable for multiple assays after a recovery period.^[16] Developed in 1947 by Argentine endocrinologist Carlos Galli-Mainini, this method requires only basic equipment, such as a syringe for injection and a microscope for observation, and demonstrates approximately 96% accuracy in detecting early pregnancy.^[15]

Advantages and Limitations

The Galli-Mainini test offered several key advantages over prior animal-based pregnancy diagnostics, primarily due to its rapid turnaround and minimal invasiveness to the test animals. Results could be obtained within 2 to 5 hours of urine injection, significantly faster than the multi-day waits required for tests like the Aschheim-Zondek or Friedman methods, enabling quicker clinical decision-making. Unlike those earlier assays, which often necessitated killing the animals to inspect ovarian changes, the Galli-Mainini test required no sacrifice; male amphibians could be reused multiple times after sperm emission, thereby reducing ethical concerns and operational costs associated with animal procurement. The procedure utilized locally abundant species, such as the South American toad Bufo arenarum in the Americas or the common European toad Bufo bufo, making it accessible without reliance on imported or scarce animals like rabbits or mice. Its low cost further enhanced its practicality in resource-limited settings. The test demonstrated high specificity, with accuracy rates reported between 95% and 97% in clinical evaluations, particularly for detecting sufficient hCG levels typical in early pregnancy, though it was less reliable for very early detection when hCG concentrations are low. Despite these strengths, the Galli-Mainini test had notable limitations that constrained its reliability and broad adoption. Accurate interpretation demanded microscopic examination to confirm sperm presence in urine, requiring trained personnel and potentially introducing operator variability, unlike simpler observational methods in some alternatives. Sensitivity varied by species, with toads generally more responsive than frogs, leading to inconsistent results depending on local availability—Bufo species outperformed Rana in responsiveness to hCG. False positives occurred due to cross-reactivity with luteinizing hormone (LH) in non-pregnant urine, such as during menstrual cycles or certain medical conditions, reducing overall precision to around 84–97% in comparative studies against the Friedman test. The assay was also less effective for early pregnancy detection before the fourth week. Historically, the test gained popularity in South America and Europe during the 1950s, where it was routinely performed in clinics and hospitals, with over 1,500 tests conducted at a single London laboratory by early 1950 alone, reflecting its integration into routine gynecological practice.^[17] To mitigate frog shortages in regions where Rana species were preferred or unavailable, variants adapted the protocol for toads, leveraging their higher sensitivity and local prevalence to maintain supply without compromising efficacy. The reusability of animals slightly alleviated ethical burdens compared to lethal tests, though modern views critique the practice as inhumane.

Decline and Legacy

Replacement by Immunological Tests

In the early 1960s, the development of immunological assays marked a pivotal shift away from animal-based pregnancy tests, enabling direct detection of human chorionic gonadotropin (hCG), the key pregnancy hormone, through antibody-antigen interactions without requiring live animals. Swedish researchers Leif Wide and Carl A. Gemzell introduced the first such test in 1960, utilizing hemagglutination inhibition, where hCG in urine samples prevented red blood cells coated with anti-hCG antibodies from clumping, providing results in a few hours with an analytical sensitivity of approximately 500 IU/L.^[1] This innovation, published in Acta Endocrinologica, laid the foundation for non-biological methods by leveraging purified hCG and rabbit-derived antibodies, achieving accuracy comparable to animal bioassays but eliminating the need for animal sacrifice.^[18] Subsequent advancements in the mid-1960s accelerated the transition. By 1967, latex agglutination tests emerged as a simpler variant, employing latex particles coated with anti-hCG antibodies that agglutinated in the presence of hCG-free urine, yielding results in under 2 minutes and suitable for clinical settings.^[19] In the 1970s, the enzyme-linked immunosorbent assay (ELISA), developed by Peter Perlmann and Eva Engvall around 1971, further refined detection by using enzyme-labeled antibodies to produce a color change proportional to hCG concentration, offering improved sensitivities compared to earlier assays.^[20] The discovery of monoclonal antibodies by Georges Köhler and César Milstein in 1975 enhanced these assays' specificity and reproducibility, as uniform antibodies reduced variability inherent in polyclonal sources.^[21] These immunological methods rapidly obsoleted animal tests due to their superior practicality and performance. Unlike animal bioassays, which required days for observation and involved ethical and logistical burdens, immunological tests delivered results in minutes, became more affordable (with home kits costing around $10 by the late 1970s), boasted high accuracy for detecting hCG at clinically relevant levels, and scaled easily for point-of-care or home use without specialized facilities.^[21] Animal-based tests, such as the Friedman rabbit assay, had peaked in usage during the 1950s, with widespread adoption in laboratories across the United States and Europe, but their demand declined sharply post-1960 as immunological alternatives proliferated.^[2] By the 1970s, most clinical settings had phased out animal methods, though limited commercial use persisted into the 1980s in some regions with slower adoption of new technologies.^[22] The transition profoundly impacted pregnancy diagnostics by reducing reliance on laboratory infrastructure and empowering individuals with immediate, private testing. The 1971 launch of Predictor, the first over-the-counter home pregnancy test in the UK, exemplified this shift, using latex agglutination inhibition to detect hCG in urine within 2 hours, thereby enhancing accessibility and confidentiality for users worldwide.^[23] This evolution not only democratized early pregnancy confirmation but also set the stage for modern rapid diagnostics.^[21]

Ethical and Environmental Impacts

The use of animals in pregnancy tests raised significant ethical concerns, particularly regarding the routine sacrifice of mammals and the stress imposed on amphibians. In the Friedman test, female rabbits were injected with urine and subsequently killed for ovarian examination, resulting in the deaths of tens of thousands of rabbits annually across diagnostic stations worldwide during the mid-20th century.^[24] This practice exemplified a violation of the 3Rs principles—replacement, reduction, and refinement—introduced in 1959, as it relied on lethal procedures without alternatives, used multiple animals per test, and caused unnecessary suffering through injections and dissection without adequate analgesia.^[25] Early animal rights activism in the 1960s highlighted these issues, with protests against vivisection contributing to broader calls for humane reforms in laboratory practices, though specific demonstrations targeted at pregnancy tests were limited.^[24] Animal welfare challenges were pronounced in both mammalian and amphibian tests. Rabbits endured pain from intravenous or intravenous injections, followed by surgical autopsy, often under ether anesthesia, a method later deemed inhumane due to its irritant effects and potential for respiratory distress.^[26] In the Hogben and Galli-Mainini tests, female Xenopus laevis or Rana pipiens frogs experienced physical stress from urine injections into the dorsal lymph sac, manifesting as muscle contractions and temporary discomfort, despite the animals' reusability every 2–3 months.^[27] These procedures contravened refinement by failing to minimize harm, prompting ethical debates on the moral cost of using sentient vertebrates for routine diagnostics. Environmentally, the mass importation of Xenopus laevis for testing from 1940 to the 1970s—exceeding 400,000 individuals from South Africa—facilitated the global spread of the chytrid fungus Batrachochytrium dendrobatidis (Bd).^[28] Trade routes introduced infected frogs to new regions, with Bd detected in U.S. populations as early as 1961, contributing to chytridiomycosis outbreaks that have driven the decline of over 500 amphibian species worldwide, including at least 90 extinctions.^[29] A 2013 study confirmed this link by analyzing preserved Xenopus specimens, revealing Bd prevalence dating back to the 1930s in South African exports used for pregnancy assays.^[30] Intensive collection also disrupted native habitats in southern Africa, exacerbating local biodiversity pressures through overharvesting and ecosystem alteration.^[28] The legacy of these tests accelerated ethical reforms, influencing the 1966 U.S. Animal Welfare Act, which mandated standards for laboratory animals and indirectly addressed vivisection concerns amid rising public scrutiny.^[31] This period's controversies spurred the transition to immunological assays in the late 1960s, aligning with 3Rs advocacy by replacing animal use with in vitro methods.^[2] Today, they inform ongoing ethical discussions in reproductive medicine, emphasizing the need to balance diagnostic utility with animal rights and ecological sustainability.^[32]

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